Widespread conservation and lineage-specific diversification of genome-wide DNA methylation patterns across arthropods

English version

Autoři: Samuel H. Lewis ^aff001; Laura Ross ^aff004; Stevie A. Bain ^aff004; Eleni Pahita ^aff002; Steven A. Smith ^aff005; Richard Cordaux ^aff006; Eric A. Miska ^aff001; Boris Lenhard ^aff002; Francis M. Jiggins ^aff001; Peter Sarkies ^aff002; Stephen A. Smith ^aff005
Působiště autorů: Department of Genetics, University of Cambridge, Cambridge, United Kingdom ^aff001; MRC London Institute of Medical Sciences, London, United Kingdom ^aff002; Institute of Clinical Sciences, Imperial College London, London, United Kingdom ^aff003; Institute of Evolutionary Biology, Edinburgh, United Kingdom ^aff004; Department of Biomedical Sciences and Pathobiology, Virginia Maryland College of Veterinary Medicine, Virginia Tech, Blacksburg, Virginia, United States of America ^aff005; Laboratoire Ecologie et Biologie des Interactions Universite de Poitiers, France ^aff006; Wellcome Trust/Cancer Research UK Gurdon Institute, Cambridge, United Kingdom ^aff007; Sars International Centre for Marine Molecular Biology, University of Bergen, Bergen, Norway ^aff008
Vyšlo v časopise: Widespread conservation and lineage-specific diversification of genome-wide DNA methylation patterns across arthropods. PLoS Genet 16(6): e32767. doi:10.1371/journal.pgen.1008864
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008864

Souhrn

Cytosine methylation is an ancient epigenetic modification yet its function and extent within genomes is highly variable across eukaryotes. In mammals, methylation controls transposable elements and regulates the promoters of genes. In insects, DNA methylation is generally restricted to a small subset of transcribed genes, with both intergenic regions and transposable elements (TEs) depleted of methylation. The evolutionary origin and the function of these methylation patterns are poorly understood. Here we characterise the evolution of DNA methylation across the arthropod phylum. While the common ancestor of the arthropods had low levels of TE methylation and did not methylate promoters, both of these functions have evolved independently in centipedes and mealybugs. In contrast, methylation of the exons of a subset of transcribed genes is ancestral and widely conserved across the phylum, but has been lost in specific lineages. A similar set of genes is methylated in all species that retained exon-enriched methylation. We show that these genes have characteristic patterns of expression correlating to broad transcription initiation sites and well-positioned nucleosomes, providing new insights into potential mechanisms driving methylation patterns over hundreds of millions of years.

Klíčová slova:

Arthropoda – DNA methylation – Drosophila melanogaster – Gene expression – Insects – Invertebrate genomics – Methylation – Nucleosomes

Zdroje

1. Holliday R, Kakutani T, Martienssen R, Richards E. The inheritance of epigenetic defects. Science. 1987;238 : 163–70. doi: 10.1126/science.3310230 3310230

2. Holliday R. Epigenetics: A historical overview. Epigenetics. 2006. pp. 76–80. doi: 10.4161/epi.1.2.2762 17998809

3. Law JA, Jacobsen SE. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nature Reviews Genetics. 2010. pp. 204–220. doi: 10.1038/nrg2719 20142834

4. Jeltsch A. Molecular enzymology of mammalian DNA methyltransferases. Current Topics in Microbiology and Immunology. 2006. pp. 203–225. doi: 10.1007/3-540-31390-7_7 16570849

5. Nashun B, Hill PWS, Hajkova P. Reprogramming of cell fate: epigenetic memory and the erasure of memories past. EMBO J. 2015;34 : 1296–308. doi: 10.15252/embj.201490649 25820261

6. Ponger L, Li WH. Evolutionary diversification of DNA methyltransferases in eukaryotic genomes. Mol Biol Evol. 2005;22 : 1119–1128. doi: 10.1093/molbev/msi098 15689527

7. Bird A. DNA methylation patterns and epigenetic memory. Genes Dev. 2002;16 : 6–21. doi: 10.1101/gad.947102 11782440

8. Walsh CP, Chaillet JR, Bestor TH. Transcription of IAP endogenous retroviruses is constrained by cytosine methylation. Nat Genet. 1998;20 : 116–117. doi: 10.1038/2413 9771701

9. Suzuki MM, Bird A. DNA methylation landscapes: provocative insights from epigenomics. Nat Rev Genet. 2008;9 : 465–476. doi: 10.1038/nrg2341 18463664

10. Zemach A, McDaniel IE, Silva P, Zilberman D. Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science (80-). 2010;328 : 916–919. doi: 10.1126/science.1186366 20395474

11. Feng S, Cokus SJ, Zhang X, Chen P-Y, Bostick M, Goll MG, et al. Conservation and divergence of methylation patterning in plants and animals. Proc Natl Acad Sci. 2010;107 : 8689–8694. doi: 10.1073/pnas.1002720107 20395551

12. Rošić S, Amouroux R, Requena CE, Gomes A, Emperle M, Beltran T, et al. Evolutionary analysis indicates that DNA alkylation damage is a byproduct of cytosine DNA methyltransferase activity. Nat Genet. 2018;50 : 452–459. doi: 10.1038/s41588-018-0061-8 29459678

13. Bewick AJ, Vogel KJ, Moore AJ, Schmitz RJ. Evolution of DNA methylation across insects. Mol Biol Evol. 2017;34 : 654–665. doi: 10.1093/molbev/msw264 28025279

14. Bewick AJ, Hofmeister BT, Powers RA, Mondo SJ, Grigoriev I V., James TY, et al. Diversity of cytosine methylation across the fungal tree of life. Nat Ecol Evol. 2019;3 : 479–490. doi: 10.1038/s41559-019-0810-9 30778188

15. de Mendoza A, Pflueger J, Lister R. Capture of a functionally active methyl-CpG binding domain by an arthropod retrotransposon family. Genome Res. 2019;29 : 1277–1286. doi: 10.1101/gr.243774.118 31239280

16. de Mendoza A, Hatleberg WL, Pang K, Leininger S, Bogdanovic O, Pflueger J, et al. Convergent evolution of a vertebrate-like methylome in a marine sponge. Nat Ecol Evol. 2019;3 : 1464–1473. doi: 10.1038/s41559-019-0983-2 31558833

17. Keller TE, Han P, Yi S V. Evolutionary transition of promoter and gene body DNA methylation across invertebrate-vertebrate boundary. Mol Biol Evol. 2016;33 : 1019–1028. doi: 10.1093/molbev/msv345 26715626

18. Wang Y, Jorda M, Jones PL, Maleszka R, Ling X, Robertson HM, et al. Functional CpG methylation system in a social insect. Science (80-). 2006;314 : 645–647. doi: 10.1126/science.1135213 17068262

19. Lyko F, Foret S, Kucharski R, Wolf S, Falckenhayn C, Maleszka R. The Honey Bee Epigenomes: Differential Methylation of Brain DNA in Queens and Workers. Keller L, editor. PLoS Biol. 2010;8: e1000506. doi: 10.1371/journal.pbio.1000506 21072239

20. Xiang H, Zhu J, Chen Q, Dai F, Li X, Li M, et al. Single base–resolution methylome of the silkworm reveals a sparse epigenomic map. Nat Biotechnol. 2010;28 : 516–520. doi: 10.1038/nbt.1626 20436463

21. Wang X, Wheeler D, Avery A, Rago A, Choi JH, Colbourne JK, et al. Function and Evolution of DNA Methylation in Nasonia vitripennis. PLoS Genet. 2013;9. doi: 10.1371/journal.pgen.1003872 24130511

22. Bonasio R, Li Q, Lian J, Mutti NS, Jin L, Zhao H, et al. Genome-wide and caste-specific DNA methylomes of the ants camponotus floridanus and harpegnathos saltator. Curr Biol. 2012;22 : 1755–1764. doi: 10.1016/j.cub.2012.07.042 22885060

23. Kao D, Lai AG, Stamataki E, Rosic S, Konstantinides N, Jarvis E, et al. The genome of the crustacean parhyale hawaiensis, a model for animal development, regeneration, immunity and lignocellulose digestion. Elife. 2016;5. doi: 10.7554/eLife.20062.001

24. Kvist J, Gonçalves Athanàsio C, Shams Solari O, Brown JB, Colbourne JK, Pfrender ME, et al. Pattern of DNA Methylation in Daphnia: Evolutionary Perspective. Genome Biol Evol. 2018;10 : 1988–2007. doi: 10.1093/gbe/evy155 30060190

25. Liu S, Aagaard A, Bechsgaard J, Bilde T. DNA Methylation Patterns in the Social Spider, Stegodyphus dumicola. Genes (Basel). 2019;10 : 137. doi: 10.3390/genes10020137 30759892

26. Gatzmann F, Falckenhayn C, Gutekunst J, Hanna K, Raddatz G, Carneiro VC, et al. The methylome of the marbled crayfish links gene body methylation to stable expression of poorly accessible genes. Epigenetics and Chromatin. 2018;11. doi: 10.1186/s13072-018-0229-6 30286795

27. Wu P, Jie W, Shang Q, Annan E, Jiang X, Hou C, et al. DNA methylation in silkworm genome may provide insights into epigenetic regulation of response to Bombyx mori cypovirus infection. Sci Rep. 2017;7 : 16013. doi: 10.1038/s41598-017-16357-7 29167521

28. Bewick AJ, Zhang Y, Wendte JM, Zhang X, Schmitz RJ. Evolutionary and experimental loss of gene body methylation and its consequence to gene expression. G3 Genes, Genomes, Genet. 2019;9 : 2441–2445. doi: 10.1534/g3.119.400365 31147389

29. Goll MG, Kirpekar F, Maggert KA, Yoder JA, Hsieh C -⁠ L, Zhang X, et al. Methylation of tRNAAsp by the DNA methyltransferase homolog Dnmt2. Science. 2006;311 : 395–8. doi: 10.1126/science.1120976 16424344

30. Falckenhayn C, Boerjan B, Raddatz G, Frohme M, Schoofs L, Lyko F. Characterization of genome methylation patterns in the desert locust Schistocerca gregaria. J Exp Biol. 2013;216 : 1423–9. doi: 10.1242/jeb.080754 23264491

31. Song J, Rechkoblit O, Bestor TH, Patel DJ. Structure of DNMT1-DNA complex reveals a role for autoinhibition in maintenance DNA methylation. Science (80-). 2011;331 : 1036–1040. doi: 10.1126/science.1195380 21163962

32. Catania S, Dumesic PA, Pimentel H, Nasif A, Stoddard CI, Burke JE, et al. Evolutionary Persistence of DNA Methylation for Millions of Years after Ancient Loss of a De Novo Methyltransferase. Cell. 2020;180 : 263–277.e20. doi: 10.1016/j.cell.2019.12.012 31955845

33. Hunt BG, Glastad KM, Yi S V., Goodisman MAD. Patterning and Regulatory Associations of DNA Methylation Are Mirrored by Histone Modifications in Insects. Genome Biol Evol. 2013;5 : 591–598. doi: 10.1093/gbe/evt030 23458712

34. Bewick AJ, Sanchez Z, Mckinney EC, Moore AJ, Moore PJ, Schmitz RJ. Dnmt1 is essential for egg production and embryo viability in the large milkweed bug, Oncopeltus fasciatus. Epigenetics Chromatin. 2019;12 : 6. doi: 10.1186/s13072-018-0246-5 30616649

35. Corrales M, Rosado A, Cortini R, Van Arensbergen J, Van Steensel B, Filion GJ. Clustering of Drosophila housekeeping promoters facilitates their expression. Genome Res. 2017;27 : 1153–1161. doi: 10.1101/gr.211433.116 28420691

36. Chodavarapu RK, Feng S, Bernatavichute Y V., Chen P-Y, Stroud H, Yu Y, et al. Relationship between nucleosome positioning and DNA methylation. Nature. 2010;466 : 388–392. doi: 10.1038/nature09147 20512117

37. Zhang L, Xie WJ, Liu S, Meng L, Gu C, Gao YQ. DNA Methylation Landscape Reflects the Spatial Organization of Chromatin in Different Cells. Biophys J. 2017;113 : 1395–1404. doi: 10.1016/j.bpj.2017.08.019 28978434

38. Ho JWK, Jung YL, Liu T, Alver BH, Lee S, Ikegami K, et al. Comparative analysis of metazoan chromatin organization. Nature. 2014;512 : 449–452. doi: 10.1038/nature13415 25164756

39. Haberle V, Lenhard B. Promoter architectures and developmental gene regulation. Seminars in Cell and Developmental Biology. 2016. doi: 10.1016/j.semcdb.2016.01.014 26783721

40. Carninci P, Sandelin A, Lenhard B, Katayama S, Shimokawa K, Ponjavic J, et al. Genome-wide analysis of mammalian promoter architecture and evolution. Nat Genet. 2006;38 : 626–635. doi: 10.1038/ng1789 16645617

41. Hoskins RA, Landolin JM, Brown JB, Sandler JE, Takahashi H, Lassmann T, et al. Genome-wide analysis of promoter architecture in Drosophila melanogaster. Genome Res. 2011;21 : 182–92. doi: 10.1101/gr.112466.110 21177961

42. Lenhard B, Sandelin A, Carninci P. Metazoan promoters: emerging characteristics and insights into transcriptional regulation. Nat Rev Genet. 2012;13 : 233–245. doi: 10.1038/nrg3163 22392219

43. Haberle V, Li N, Hadzhiev Y, Plessy C, Previti C, Nepal C, et al. Two independent transcription initiation codes overlap on vertebrate core promoters. Nature. 2014;507 : 381–385. doi: 10.1038/nature12974 24531765

44. Quenneville S, Turelli P, Bojkowska K, Raclot C, Offner S, Kapopoulou A, et al. The KRAB-ZFP/KAP1 system contributes to the early embryonic establishment of site-specific DNA methylation patterns maintained during development. Cell Rep. 2012;2 : 766–73. doi: 10.1016/j.celrep.2012.08.043 23041315

45. Dixon GB, Bay LK, Matz M V. Evolutionary Consequences of DNA Methylation in a Basal Metazoan. Mol Biol Evol. 2016;33 : 2285–2293. doi: 10.1093/molbev/msw100 27189563

46. Takuno S, Gaut BS. Gene body methylation is conserved between plant orthologs and is of evolutionary consequence. Proc Natl Acad Sci U S A. 2013;110 : 1797–1802. doi: 10.1073/pnas.1215380110 23319627

47. Takuno S, Ran JH, Gaut BS. Evolutionary patterns of genic DNA methylation vary across land plants. Nat Plants. 2016;2 : 1–7. doi: 10.1038/NPLANTS.2015.222 27249194

48. Bewick AJ, Schmitz RJ. Gene body DNA methylation in plants. Current Opinion in Plant Biology. 2017. doi: 10.1016/j.pbi.2016.12.007 28258985

49. Seymour DK, Gaut BS. Phylogenetic Shifts in Gene Body Methylation Correlate with Gene Expression and Reflect Trait Conservation. Purugganan M, editor. Mol Biol Evol. 2020;37 : 31–43. doi: 10.1093/molbev/msz195 31504743

50. Bewick AJ, Ji L, Niederhuth CE, Willing EM, Hofmeister BT, Shi X, et al. On the origin and evolutionary consequences of gene body DNA methylation. Proc Natl Acad Sci U S A. 2016;113 : 9111–9116. doi: 10.1073/pnas.1604666113 27457936

51. Muyle A, Gaut BS. Loss of Gene Body Methylation in Eutrema salsugineum Is Associated with Reduced Gene Expression. Purugganan M, editor. Mol Biol Evol. 2019;36 : 155–158. doi: 10.1093/molbev/msy204 30398664

52. Zilberman D. An evolutionary case for functional gene body methylation in plants and animals. Genome Biol. 2017;18 : 87. doi: 10.1186/s13059-017-1230-2 28486944

53. Morselli M, Pastor WA, Montanini B, Nee K, Ferrari R, Fu K, et al. In vivo targeting of de novo DNA methylation by histone modifications in yeast and mouse. Elife. 2015;4. doi: 10.7554/eLife.06205 25848745

54. Baubec T, Colombo DF, Wirbelauer C, Schmidt J, Burger L, Krebs AR, et al. Genomic profiling of DNA methyltransferases reveals a role for DNMT3B in genic methylation. Nature. 2015;520 : 243–247. doi: 10.1038/nature14176 25607372

55. Schwartz S, Meshorer E, Ast G. Chromatin organization marks exon-intron structure. Nat Struct Mol Biol. 2009;16 : 990–995. doi: 10.1038/nsmb.1659 19684600

56. Tilgner H, Nikolaou C, Althammer S, Sammeth M, Beato M, Valcárcel J, et al. Nucleosome positioning as a determinant of exon recognition. Nat Struct Mol Biol. 2009;16 : 996–1001. doi: 10.1038/nsmb.1658 19684599

57. Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods. 2015;12 : 59–60. doi: 10.1038/nmeth.3176 25402007

58. Castresana J. Selection of Conserved Blocks from Multiple Alignments for Their Use in Phylogenetic Analysis. Mol Biol Evol. 2000;17 : 540–552. doi: 10.1093/oxfordjournals.molbev.a026334 10742046

59. Jones P, Binns D, Chang H-Y, Fraser M, Li W, McAnulla C, et al. InterProScan 5: genome-scale protein function classification. Bioinformatics. 2014;30 : 1236–1240. doi: 10.1093/bioinformatics/btu031 24451626

60. Lagesen K, Hallin P, Rødland EA, Stærfeldt H -⁠ H, Rognes T, Ussery DW. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res. 2007;35 : 3100–3108. doi: 10.1093/nar/gkm160 17452365

61. Lowe TM, Eddy SR. tRNAscan-SE: A Program for Improved Detection of Transfer RNA Genes in Genomic Sequence. Nucleic Acids Res. 1997;25 : 955–964. doi: 10.1093/nar/25.5.955 9023104

62. Galbraith DA, Yang X, Niño EL, Yi S, Grozinger C. Parallel Epigenomic and Transcriptomic Responses to Viral Infection in Honey Bees (Apis mellifera). Schneider DS, editor. PLOS Pathog. 2015;11: e1004713. doi: 10.1371/journal.ppat.1004713 25811620

63. Krueger F, Andrews SR. Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics. 2011;27 : 1571–1572. doi: 10.1093/bioinformatics/btr167 21493656

64. Barturen G, Rueda A, Oliver JL, Hackenberg M. MethylExtract: High-Quality methylation maps and SNV calling from whole genome bisulfite sequencing data. F1000Research. 2014;2 : 217. doi: 10.12688/f1000research.2-217.v2 24627790

65. Revell LJ. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol. 2012;3 : 217–223. doi: 10.1111/j.2041-210X.2011.00169.x

66. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30. doi: 10.1093/molbev/mst010 23329690

67. Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian Phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol. 2012;29 : 1969–1973. doi: 10.1093/molbev/mss075 22367748

68. Misof B, Liu S, Meusemann K, Peters RS, Donath A, Mayer C, et al. Phylogenomics resolves the timing and pattern of insect evolution. Science. 2014;346 : 763–7. doi: 10.1126/science.1257570 25378627

69. Hadfield JD. MCMC Methods for Multi-Response Generalized Linear Mixed Models: The MCMCglmm R Package. J Stat Softw. 2010;33 : 1–22. doi: 10.18637/jss.v033.i02 20808728

70. Lewis SH, Quarles KA, Yang Y, Tanguy M, Frézal L, Smith SA, et al. Pan-arthropod analysis reveals somatic piRNAs as an ancestral defence against transposable elements. Nat Ecol Evol. 2018;2 : 174–181. doi: 10.1038/s41559-017-0403-4 29203920

71. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 2013;14: R36. doi: 10.1186/gb-2013-14-4-r36 23618408

72. Murata M, Nishiyori-Sueki H, Kojima-Ishiyama M, Carninci P, Hayashizaki Y, Itoh M. Detecting expressed genes using CAGE. Methods Mol Biol. 2014. doi: 10.1007/978-1-4939-0805-9_7 24927836

73. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Meth. 2012;9 : 357–359. Available: http://dx.doi.org/10.1038/nmeth.1923

74. Haberle V, Forrest ARR, Hayashizaki Y, Carninci P, Lenhard B. CAGEr: Precise TSS data retrieval and high-resolution promoterome mining for integrative analyses. Nucleic Acids Res. 2015. doi: 10.1093/nar/gkv054 25653163

Článek Duplication and divergence of the retrovirus restriction gene Fv1 in Mus caroli allows protection from multiple retroviruses

Článek Super-resolution imaging of RAD51 and DMC1 in DNA repair foci reveals dynamic distribution patterns in meiotic prophase

Článek Steroid hormones regulate genome-wide epigenetic programming and gene transcription in human endometrial cells with marked aberrancies in endometriosis

Článek Regulation of olfactory-based sex behaviors in the silkworm by genes in the sex-determination cascade

Článek Osteocalcin promotes bone mineralization but is not a hormone

Článek A conserved, N-terminal tyrosine signal directs Ras for inhibition by Rabex-5

Článek Integrins regulate epithelial cell shape by controlling the architecture and mechanical properties of basal actomyosin networks

Článek Cancer-associated mutations in the iron-sulfur domain of FANCJ affect G-quadruplex metabolism

Článek NRF2 loss recapitulates heritable impacts of paternal cigarette smoke exposure

Článek Pax6 organizes the anterior eye segment by guiding two distinct neural crest waves

Článek Transcriptomic stratification of late-onset Alzheimer's cases reveals novel genetic modifiers of disease pathology

Článek Alpha- and beta-adrenergic octopamine receptors in muscle and heart are required for Drosophila exercise adaptations