Local Effect of Enhancer of Zeste-Like Reveals Cooperation of Epigenetic and -Acting Determinants for Zygotic Genome Rearrangements

English version České info

The unicellular eukaryote Paramecium tetraurelia provides an extraordinary model for studying the mechanisms involved in zygotic genome rearrangements. At each sexual cycle, differentiation of the somatic nucleus from the zygotic nucleus is characterized by extensive remodeling of the entire somatic genome, which includes the precise excision of 45,000 short noncoding germline DNA segments to reconstitute functional open reading frames. Exploiting the unique properties of the Paramecium genome, we show that the enhancer of zeste like protein Ezl1 is necessary for histone H3 trimethylation on lysines 27 and 9 and is required for the precise excision of 31,000 of these single copy, dispersed germline DNA segments that can be as short as 26 bp in length. This implies that histone marks usually associated with heterochromatin may contribute to the precise demarcation of segments that are even shorter than the length of DNA wrapped around a single nucleosome. A quantitative analysis of high throughput sequencing datasets further shows that the underlying genetic properties of the germline DNA segments might act in concert with epigenetic signals to define germline specific sequences.

Vyšlo v časopise: Local Effect of Enhancer of Zeste-Like Reveals Cooperation of Epigenetic and -Acting Determinants for Zygotic Genome Rearrangements. PLoS Genet 10(9): e32767. doi:10.1371/journal.pgen.1004665
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004665

Souhrn

Zdroje

1. ChalkerDL, YaoMC (2011) DNA elimination in ciliates: transposon domestication and genome surveillance. Annu Rev Genet 45: 227–246.

2. ArnaizO, MathyN, BaudryC, MalinskyS, AuryJ-M, et al. (2012) The Paramecium germline genome provides a niche for intragenic parasitic DNA: evolutionary dynamics of internal eliminated sequences. PLoS Genet 8: e1002984 doi:10.1371/journal.pgen.1002984

3. BaudryC, MalinskyS, RestituitoM, KapustaA, RosaS, et al. (2009) PiggyMac, a domesticated piggyBac transposase involved in programmed genome rearrangements in the ciliate Paramecium tetraurelia. Genes Dev 23: 2478–2483.

4. KlobutcherLA, HerrickG (1995) Consensus inverted terminal repeat sequence of Paramecium IESs: resemblance to termini of Tc1-related and Euplotes Tec transposons. Nucleic Acids Res 23: 2006–2013.

5. LepereG, NowackiM, SerranoV, GoutJF, GuglielmiG, et al. (2009) Silencing-associated and meiosis-specific small RNA pathways in Paramecium tetraurelia. Nucleic Acids Res 37: 903–915.

6. SandovalPY, SwartEC, ArambasicM, NowackiM (2014) Functional Diversification of Dicer-like Proteins and Small RNAs Required for Genome Sculpting. Dev Cell 28: 174–188 doi:10.1016/j.devcel.2013.12.010

7. LepereG, BetermierM, MeyerE, DuharcourtS (2008) Maternal noncoding transcripts antagonize the targeting of DNA elimination by scanRNAs in Paramecium tetraurelia. Genes Dev 22: 1501–1512.

8. DuharcourtS, LepereG, MeyerE (2009) Developmental genome rearrangements in ciliates: a natural genomic subtraction mediated by non-coding transcripts. Trends Genet 25: 344–350.

9. CoyneRS, Lhuillier-AkakpoM, DuharcourtS (2012) RNA-guided DNA rearrangements in ciliates: Is the best genome defence a good offence? Biol Cell 104: 1–17 doi:10.1111/boc.201100057

10. DuharcourtS, ButlerA, MeyerE (1995) Epigenetic self-regulation of developmental excision of an internal eliminated sequence on Paramecium tetraurelia. Genes Dev 9: 2065–2077.

11. DuharcourtS, KellerAM, MeyerE (1998) Homology-dependent maternal inhibition of developmental excision of internal eliminated sequences in Paramecium tetraurelia. Mol Cell Biol 18: 7075–7085.

12. GarnierO, SerranoV, DuharcourtS, MeyerE (2004) RNA-mediated programming of developmental genome rearrangements in Paramecium tetraurelia. Mol Cell Biol 24: 7370–7379.

13. Singh DP, Saudemont B, Guglielmi G, Arnaiz O, Goût J-F, et al. (2014) Genome-defence small RNAs exapted for epigenetic mating-type inheritance. Nature In press. Available: http://dx.doi.org/10.1038/_nature13318.

14. TavernaSD, CoyneRS, AllisCD (2002) Methylation of histone h3 at lysine 9 targets programmed DNA elimination in tetrahymena. Cell 110: 701–711.

15. LiuY, MochizukiK, GorovskyMA (2004) Histone H3 lysine 9 methylation is required for DNA elimination in developing macronuclei in Tetrahymena. Proc Natl Acad Sci U A 101: 1679–1684.

16. LiuY, TavernaSD, MuratoreTL, ShabanowitzJ, HuntDF, et al. (2007) RNAi-dependent H3K27 methylation is required for heterochromatin formation and DNA elimination in Tetrahymena. Genes Dev 21: 1530–1545.

17. MaloneCD, AndersonAM, MotlJA, RexerCH, ChalkerDL (2005) Germ line transcripts are processed by a Dicer-like protein that is essential for developmentally programmed genome rearrangements of Tetrahymena thermophila. Mol Cell Biol 25: 9151–9164.

18. ChengCY, VogtA, MochizukiK, YaoMC (2010) A domesticated piggyBac transposase plays key roles in heterochromatin dynamics and DNA cleavage during programmed DNA deletion in Tetrahymena thermophila. Mol Biol Cell 21: 1753–1762.

19. VogtA, MochizukiK (2013) A domesticated PiggyBac transposase interacts with heterochromatin and catalyzes reproducible DNA elimination in Tetrahymena. PLoS Genet 9: e1004032 doi:10.1371/journal.pgen.1004032

20. CastelSE, MartienssenRA (2013) RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond. Nat Rev Genet 14: 100–112 doi:10.1038/nrg3355

21. GeDT, ZamorePD (2013) Small RNA-Directed Silencing: The Fly Finds Its Inner Fission Yeast? Curr Biol 23: R318–R320 doi:10.1016/j.cub.2013.03.033

22. FassJN, JoshiNA, CouvillionMT, BowenJ, GorovskyMA, et al. (2011) Genome-Scale Analysis of Programmed DNA Elimination Sites in Tetrahymena thermophila. G3 Bethesda Md 1: 515–522 doi:10.1534/g3.111.000927

23. MadireddiMT, CoyneRS, SmothersJF, MickeyKM, YaoMC, et al. (1996) Pdd1p, a novel chromodomain-containing protein, links heterochromatin assembly and DNA elimination in Tetrahymena. Cell 87: 75–84.

24. GreerEL, ShiY (2012) Histone methylation: a dynamic mark in health, disease and inheritance. Nat Rev Genet 13: 343–357 doi:10.1038/nrg3173

25. AuryJM, JaillonO, DuretL, NoelB, JubinC, et al. (2006) Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature 444: 171–178.

26. ArnaizO, GoutJF, BetermierM, BouhoucheK, CohenJ, et al. (2010) Gene expression in a paleopolyploid: a transcriptome resource for the ciliate Paramecium tetraurelia. BMC Genomics 11: 547.

27. BouhoucheK, GoutJF, KapustaA, BetermierM, MeyerE (2011) Functional specialization of Piwi proteins in Paramecium tetraurelia from post-transcriptional gene silencing to genome remodelling. Nucleic Acids Res 39: 4249–4264.

28. NowackiM, Zagorski-OstojaW, MeyerE (2005) Nowa1p and Nowa2p: novel putative RNA binding proteins involved in trans-nuclear crosstalk in Paramecium tetraurelia. Curr Biol 15: 1616–1628.

29. NowakJK, GromadkaR, JuszczukM, Jerka-DziadoszM, MaliszewskaK, et al. (2011) A functional study of genes essential for autogamy and nuclear reorganization in Paramecium.. Eukaryot Cell 10: 363–72.

30. BetermierM, DuharcourtS, SeitzH, MeyerE (2000) Timing of developmentally programmed excision and circularization of Paramecium internal eliminated sequences. Mol Cell Biol 20: 1553–1561.

31. MieleV, VaillantC, d’ Aubenton-CarafaY, ThermesC, GrangeT (2008) DNA physical properties determine nucleosome occupancy from yeast to fly. Nucleic Acids Res 36: 3746–3756 doi:10.1093/nar/gkn262

32. PeckhamHE, ThurmanRE, FuY, StamatoyannopoulosJA, NobleWS, et al. (2007) Nucleosome positioning signals in genomic DNA. Genome Res 17: 1170–1177 doi:10.1101/gr.6101007

33. LeeW, TilloD, BrayN, MorseRH, DavisRW, et al. (2007) A high-resolution atlas of nucleosome occupancy in yeast. Nat Genet 39: 1235–1244.

34. SiomiMC, SatoK, PezicD, AravinAA (2011) PIWI-interacting small RNAs: the vanguard of genome defence. Nat Rev Mol Cell Biol 12: 246–258.

35. MaloneCD, HannonGJ (2009) Small RNAs as guardians of the genome. Cell 136: 656–668.

36. MargueronR, ReinbergD (2011) The Polycomb complex PRC2 and its mark in life. Nature 469: 343–349 doi:10.1038/nature09784

37. SzerlongHJ, HansenJC (2011) Nucleosome distribution and linker DNA: connecting nuclear function to dynamic chromatin structure. Biochem Cell Biol Biochim Biol Cell 89: 24–34 doi:10.1139/O10-139

38. RanjanA, MizuguchiG, FitzGeraldPC, WeiD, WangF, et al. (2013) Nucleosome-free region dominates histone acetylation in targeting SWR1 to promoters for H2A.Z replacement. Cell 154: 1232–1245 doi:10.1016/j.cell.2013.08.005

39. Beisson J, Betermier M, Bre MH, Cohen J, Duharcourt S, et al. (2010) Maintaining clonal Paramecium tetraurelia cell lines of controlled age through daily reisolation. Cold Spring Harb Protoc 2010: pdb prot5361.

40. BeissonJ, BetermierM, BreMH, CohenJ, DuharcourtS, et al. (2010) (2010) Mass culture of Paramecium tetraurelia. Cold Spring Harb Protoc pdb prot5362.

41. PuntaM, CoggillPC, EberhardtRY, MistryJ, TateJ, et al. (2012) The Pfam protein families database. Nucleic Acids Res 40: D290–301 doi:10.1093/nar/gkr1065

42. AltschulSF, GishW, MillerW, MyersEW, LipmanDJ (1990) Basic local alignment search tool. J Mol Biol 215: 403–410 doi:10.1016/S0022-2836(05)80360-2

43. EdgarRC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792–1797 doi:10.1093/nar/gkh340

44. GuindonS, GascuelO (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696–704.

45. GuindonS, LethiecF, DurouxP, GascuelO (2005) PHYML Online—a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res 33: W557–559 doi:10.1093/nar/gki352

46. LeSQ, GascuelO (2008) An improved general amino acid replacement matrix. Mol Biol Evol 25: 1307–1320 doi:10.1093/molbev/msn067

47. AnisimovaM, GascuelO (2006) Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. Syst Biol 55: 539–552 doi:10.1080/10635150600755453

48. GalvaniA, SperlingL (2002) RNA interference by feeding in Paramecium. Trends Genet 18: 11–12.

49. ArnaizO, SperlingL (2011) ParameciumDB in 2011: new tools and new data for functional and comparative genomics of the model ciliate Paramecium tetraurelia. Nucleic Acids Res 39: D632–636 doi:10.1093/nar/gkq918

50. ShechterD, DormannHL, AllisCD, HakeSB (2007) Extraction, purification and analysis of histones. Nat Protoc 2: 1445–1457.

51. LiH, DurbinR (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinforma Oxf Engl 25: 1754–1760 doi:10.1093/bioinformatics/btp324

52. LiH, HandsakerB, WysokerA, FennellT, RuanJ, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinforma Oxf Engl 25: 2078–2079 doi:10.1093/bioinformatics/btp352

53. Dorai-Raj S (2009) binom: Binomial Confidence Intervals For Several Parameterizations. R package version 1.0-5. http://CRAN.R-project.org/package=binom.

54. BenjaminiY, HochbergY (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing;. J R Stat Soc Ser B 57: 289–300.

55. MadedduL, GautierMC, VayssieL, HouariA, SperlingL (1995) A large multigene family codes for the polypeptides of the crystalline trichocyst matrix in Paramecium. Mol Biol Cell 6: 649–659.

56. GogendeauD, KlotzC, ArnaizO, MalinowskaA, DadlezM, et al. (2008) Functional diversification of centrins and cell morphological complexity. J Cell Sci 121: 65–74 doi:10.1242/jcs.019414

57. BergerJD (1986) Autogamy in Paramecium. Cell cycle stage-specific commitment to meiosis. Exp Cell Res 166: 475–485.

58. SunX-J, XuP-F, ZhouT, HuM, FuC-T, et al. (2008) Genome-wide survey and developmental expression mapping of zebrafish SET domain-containing genes. PloS One 3: e1499 doi:10.1371/journal.pone.0001499

59. ZhangL, MaH (2012) Complex evolutionary history and diverse domain organization of SET proteins suggest divergent regulatory interactions. New Phytol 195: 248–263 doi:10.1111/j.1469-8137.2012.04143.x

60. DillonSC, ZhangX, TrievelRC, ChengX (2005) The SET-domain protein superfamily: protein lysine methyltransferases. Genome Biol 6: 227 doi:10.1186/gb-2005-6-8-227

61. JoshiP, CarringtonEA, WangL, KetelCS, MillerEL, et al. (2008) Dominant alleles identify SET domain residues required for histone methyltransferase of Polycomb repressive complex 2. J Biol Chem 283: 27757–27766 doi:10.1074/jbc.M804442200