#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Century-scale Methylome Stability in a Recently Diverged Lineage


It continues to be hotly debated to what extent environmentally induced epigenetic change is stably inherited and thereby contributes to short-term adaptation. It has been shown before that natural Arabidopsis thaliana lines differ substantially in their methylation profiles. How much of this is independent of genetic changes remains, however, unclear, especially given that there is very little conservation of methylation between species, simply because the methylated sequences themselves, mostly repeats, are not conserved over millions of years. On the other hand, there is no doubt that artificially induced epialleles can contribute to phenotypic variation. To investigate whether epigenetic differentiation, at least in the short term, proceeds very differently from genetic variation, and whether genome-wide epigenetic fingerprints can be used to uncover local adaptation, we have taken advantage of a near-clonal North American A. thaliana population that has diverged under natural conditions for at least a century. We found that both patterns and rates of methylome variation were in many aspects similar to those of lines grown in stable environments, which suggests that environment-induced changes are only minor contributors to durable genome-wide heritable epigenetic variation.


Vyšlo v časopise: Century-scale Methylome Stability in a Recently Diverged Lineage. PLoS Genet 11(1): e32767. doi:10.1371/journal.pgen.1004920
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004920

Souhrn

It continues to be hotly debated to what extent environmentally induced epigenetic change is stably inherited and thereby contributes to short-term adaptation. It has been shown before that natural Arabidopsis thaliana lines differ substantially in their methylation profiles. How much of this is independent of genetic changes remains, however, unclear, especially given that there is very little conservation of methylation between species, simply because the methylated sequences themselves, mostly repeats, are not conserved over millions of years. On the other hand, there is no doubt that artificially induced epialleles can contribute to phenotypic variation. To investigate whether epigenetic differentiation, at least in the short term, proceeds very differently from genetic variation, and whether genome-wide epigenetic fingerprints can be used to uncover local adaptation, we have taken advantage of a near-clonal North American A. thaliana population that has diverged under natural conditions for at least a century. We found that both patterns and rates of methylome variation were in many aspects similar to those of lines grown in stable environments, which suggests that environment-induced changes are only minor contributors to durable genome-wide heritable epigenetic variation.


Zdroje

1. MartinA, TroadecC, BoualemA, RajabM, FernandezR, et al. (2009) A transposon-induced epigenetic change leads to sex determination in melon. Nature 461: 1135–1138.

2. WangX, WeigelD, SmithLM (2013) Transposon variants and their effects on gene expression in Arabidopsis. PLoS Genet 9: e1003255.

3. BenderJ, FinkGR (1995) Epigenetic control of an endogenous gene family is revealed by a novel blue fluorescent mutant of Arabidopsis. Cell 83: 725–734.

4. MelquistS, LuffB, BenderJ (1999) Arabidopsis PAI gene arrangements, cytosine methylation and expression. Genetics 153: 401–413.

5. SilveiraAB, TrontinC, CortijoS, BarauJ, Del BemLE, et al. (2013) Extensive natural epigenetic variation at a de novo originated gene. PLoS Genet 9: e1003437.

6. GanX, StegleO, BehrJ, SteffenJG, DreweP, et al. (2011) Multiple reference genomes and transcriptomes for Arabidopsis thaliana. Nature 477: 419–423.

7. CaoJ, SchneebergerK, OssowskiS, GuntherT, BenderS, et al. (2011) Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nat Genet 43: 956–963.

8. SchneebergerK, OssowskiS, OttF, KleinJD, WangX, et al. (2011) Reference-guided assembly of four diverse Arabidopsis thaliana genomes. Proc Natl Acad Sci USA 108: 10249–10254.

9. LongQ, RabanalFA, MengD, HuberCD, FarlowA, et al. (2013) Massive genomic variation and strong selection in Arabidopsis thaliana lines from Sweden. Nat Genet 45: 884–890.

10. SchmitzRJ, SchultzMD, UrichMA, NeryJR, PelizzolaM, et al. (2013) Patterns of population epigenomic diversity. Nature 495: 193–198.

11. RichardsEJ (2006) Inherited epigenetic variation – revisiting soft inheritance. Nature reviews Genetics 7: 395–401.

12. BeckerC, HagmannJ, MüllerJ, KoenigD, StegleO, et al. (2011) Spontaneous epigenetic variation in the Arabidopsis thaliana methylome. Nature 480: 245–249.

13. SchmitzRJ, SchultzMD, LewseyMG, O'MalleyRC, UrichMA, et al. (2011) Transgenerational epigenetic instability is a source of novel methylation variants. Science 334: 369–373.

14. AlabertC, GrothA (2012) Chromatin replication and epigenome maintenance. Nat Rev Mol Cell Biol 13: 153–167.

15. GenereuxDP, MinerBE, BergstromCT, LairdCD (2005) A population-epigenetic model to infer site-specific methylation rates from double-stranded DNA methylation patterns. Proc Natl Acad Sci USA 102: 5802–5807.

16. LiuQ, GongZ (2011) The coupling of epigenome replication with DNA replication. Curr Opin Plant Biol 14: 187–194.

17. LawJA, JacobsenSE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11: 204–220.

18. CalarcoJP, BorgesF, DonoghueMT, Van ExF, JullienPE, et al. (2012) Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA. Cell 151: 194–205.

19. TeixeiraFK, HerediaF, SarazinA, RoudierF, BoccaraM, et al. (2009) A role for RNAi in the selective correction of DNA methylation defects. Science 323: 1600–1604.

20. LatzelV, AllanE, Bortolini SilveiraA, ColotV, FischerM, et al. (2013) Epigenetic diversity increases the productivity and stability of plant populations. Nat Commun 4: 2875.

21. RouxF, Colomé-TatchéM, EdelistC, WardenaarR, GuercheP, et al. (2011) Genome-wide epigenetic perturbation jump-starts patterns of heritable variation found in nature. Genetics 188: 1015–1017.

22. Cortijo S, Wardenaar R, Colome-Tatche M, Gilly A, Etcheverry M, et al.. (2014) Mapping the epigenetic basis of complex traits. Science: ePub Feb 06, 2014.

23. DowenRH, PelizzolaM, SchmitzRJ, ListerR, DowenJM, et al. (2012) Widespread dynamic DNA methylation in response to biotic stress. Proc Natl Acad Sci U S A 109: E2183–2191.

24. BondurianskyR (2012) Rethinking heredity, again. Trends Ecol Evol 27: 330–336.

25. BossdorfO, RichardsCL, PigliucciM (2008) Epigenetics for ecologists. Ecol Lett 11: 106–115.

26. DanchinE, CharmantierA, ChampagneFA, MesoudiA, PujolB, et al. (2011) Beyond DNA: integrating inclusive inheritance into an extended theory of evolution. Nat Rev Genet 12: 475–486.

27. JablonkaE, RazG (2009) Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. Q Rev Biol 84: 131–176.

28. BergmanY, CedarH (2013) DNA methylation dynamics in health and disease. Nat Struct Mol Biol 20: 274–281.

29. FeilR, FragaMF (2011) Epigenetics and the environment: emerging patterns and implications. Nat Rev Genet 13: 97–109.

30. GeogheganJL, SpencerHG (2012) Population-epigenetic models of selection. Theor Popul Biol 81: 232–242.

31. DaxingerL, WhitelawE (2012) Understanding transgenerational epigenetic inheritance via the gametes in mammals. Nat Rev Genet 13: 153–162.

32. MirouzeM, PaszkowskiJ (2011) Epigenetic contribution to stress adaptation in plants. Curr Opin Plant Biol 14: 267–274.

33. PaszkowskiJ, GrossniklausU (2011) Selected aspects of transgenerational epigenetic inheritance and resetting in plants. Curr Opin Plant Biol 14: 195–203.

34. BeckerC, WeigelD (2012) Epigenetic variation: origin and transgenerational inheritance. Curr Opin Plant Biol 15: 562–567.

35. PlattA, HortonM, HuangYS, LiY, AnastasioAE, et al. (2010) The scale of population structure in Arabidopsis thaliana. PLoS Genet 6: e1000843.

36. OssowskiS, SchneebergerK, Lucas-LledoJI, WarthmannN, ClarkRM, et al. (2010) The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science 327: 92–94.

37. O'KaneSL, Al-ShehbazIA (1997) A synopsis of Arabidopsis (Brassicaceae). Novon 7: 323–327.

38. ZhangX, YazakiJ, SundaresanA, CokusS, ChanSW, et al. (2006) Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126: 1189–1201.

39. JiangC, MithaniA, BelfieldEJ, MottR, HurstLD, et al. (2014) Environmentally responsive genome-wide accumulation of de novo Arabidopsis thaliana mutations and epimutations. Genome Res 24: 1821–1829.

40. SeifertM, CortijoS, Colomé-TatchéM, JohannesF, RoudierF, et al. (2012) MeDIP-HMM: genome-wide identification of distinct DNA methylation states from high-density tiling arrays. Bioinformatics 28: 2930–2939.

41. MolaroA, HodgesE, FangF, SongQ, McCombieWR, et al. (2011) Sperm methylation profiles reveal features of epigenetic inheritance and evolution in primates. Cell 146: 1029–1041.

42. Coleman-DerrD, ZilbermanD (2012) Deposition of histone variant H2A. Z within gene bodies regulates responsive genes. PLoS Genet 8: e1002988.

43. StroudH, GreenbergMV, FengS, BernatavichuteYV, JacobsenSE (2013) Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell 152: 352–364.

44. DaxingerL, WhitelawE (2012) Understanding transgenerational epigenetic inheritance via the gametes in mammals. Nat Rev Genet 13: 153–162.

45. ManolioTA, CollinsFS, CoxNJ, GoldsteinDB, HindorffLA, et al. (2009) Finding the missing heritability of complex diseases. Nature 461: 747–753.

46. SlatkinM (2009) Epigenetic inheritance and the missing heritability problem. Genetics 182: 845–850.

47. SeymourDK, KoenigD, HagmannJ, BeckerC, WeigelD (2014) Evolution of DNA Methylation Patterns in the Brassicaceae is Driven by Differences in Genome Organization. PLoS Genet 10: e1004785.

48. TakunoS, GautBS (2012) Body-methylated genes in Arabidopsis thaliana are functionally important and evolve slowly. Mol Biol Evol 29: 219–227.

49. OssowskiS, SchneebergerK, ClarkRM, LanzC, WarthmannN, et al. (2008) Sequencing of natural strains of Arabidopsis thaliana with short reads. Genome Res 18: 2024–2033.

50. SchneebergerK, HagmannJ, OssowskiS, WarthmannN, GesingS, et al. (2009) Simultaneous alignment of short reads against multiple genomes. Genome Biol 10: R98.

51. MillsRE, WalterK, StewartC, HandsakerRE, ChenK, et al. (2011) Mapping copy number variation by population-scale genome sequencing. Nature 470: 59–65.

52. YeK, SchulzMH, LongQ, ApweilerR, NingZ (2009) Pindel: a pattern growth approach to detect break points of large deletions and medium sized insertions from paired-end short reads. Bioinformatics 25: 2865–2871.

53. RauschT, ZichnerT, SchlattlA, StützAM, BenesV, et al. (2012) DELLY: structural variant discovery by integrated paired-end and split-read analysis. Bioinformatics 28: i333–i339.

54. GrimmD, HagmannJ, KoenigD, WeigelD, BorgwardtK (2013) Accurate indel prediction using paired-end short reads. BMC Genomics 14: 132.

55. LiH, DurbinR (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754–1760.

56. LuoR, LiuB, XieY, LiZ, HuangW, et al. (2012) SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. GigaScience 1: 18.

57. ZerbinoDR, BirneyE (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18: 821–829.

58. AltschulSF, GishW, MillerW, MyersEW, LipmanDJ (1990) Basic local alignment search tool. J Mol Biol 215: 403–410.

59. AlbersCA, LunterG, MacArthurDG, McVeanG, OuwehandWH, et al. (2011) Dindel: accurate indel calls from short-read data. Genome Res 21: 961–973.

60. StoreyJD, TibshiraniR (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci USA 100: 9440–9445.

61. Ionita-LazaI, LangeC, NML (2009) Estimating the number of unseen variants in the human genome. Proc Natl Acad Sci USA 106: 5008–5013.

62. RegulskiM, LuZ, KendallJ, DonoghueMT, ReindersJ, et al. (2013) The maize methylome influences mRNA splice sites and reveals widespread paramutation-like switches guided by small RNA. Genome Res 23: 1651–1662.

63. KangHM, SulJH, ServiceSK, ZaitlenNA, KongSY, et al. (2010) Variance component model to account for sample structure in genome-wide association studies. Nat Genet 42: 348–354.

64. LippertC, ListgartenJ, LiuY, KadieCM, DavidsonRI, et al. (2011) FaST linear mixed models for genome-wide association studies. Nat Methods 8: 833–835.

65. SchneebergerK, OssowskiS, LanzC, JuulT, PetersenAH, et al. (2009) SHOREmap: simultaneous mapping and mutation identification by deep sequencing. Nat Methods 6: 550–551.

66. PritchardJK, StephensM, DonnellyP (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945–959.

67. EvannoG, RegnautS, GoudetJ (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14: 2611–2620.

68. HusonDH, BryantD (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23: 254–267.

69. SlotteT, HazzouriKM, AgrenJA, KoenigD, MaumusF, et al. (2013) The Capsella rubella genome and the genomic consequences of rapid mating system evolution. Nat Genet 45: 831–835.

70. KimD, PerteaG, TrapnellC, PimentelH, KelleyR, et al. (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14: R36.

71. LangmeadB, SalzbergSL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9: 357–359.

72. TrapnellC, HendricksonDG, SauvageauM, GoffL, RinnJL, et al. (2013) Differential analysis of gene regulation at transcript resolution with RNA-seq. Nat Biotechnol 31: 46–53.

73. KrzywinskiM, ScheinJ, BirolI, ConnorsJ, GascoyneR, et al. (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19: 1639–1645.

74. KlukasC, PapeJM, EntzianA (2012) Analysis of high-throughput plant image data with the information system IAP. J Integr Bioinform 9: 191.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2015 Číslo 1
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#