Heritable Epigenetic Variation among Maize Inbreds
Epigenetic variation describes heritable differences that are not attributable to changes in DNA sequence. There is the potential for pure epigenetic variation that occurs in the absence of any genetic change or for more complex situations that involve both genetic and epigenetic differences. Methylation of cytosine residues provides one mechanism for the inheritance of epigenetic information. A genome-wide profiling of DNA methylation in two different genotypes of Zea mays (ssp. mays), an organism with a complex genome of interspersed genes and repetitive elements, allowed the identification and characterization of examples of natural epigenetic variation. The distribution of DNA methylation was profiled using immunoprecipitation of methylated DNA followed by hybridization to a high-density tiling microarray. The comparison of the DNA methylation levels in the two genotypes, B73 and Mo17, allowed for the identification of approximately 700 differentially methylated regions (DMRs). Several of these DMRs occur in genomic regions that are apparently identical by descent in B73 and Mo17 suggesting that they may be examples of pure epigenetic variation. The methylation levels of the DMRs were further studied in a panel of near-isogenic lines to evaluate the stable inheritance of the methylation levels and to assess the contribution of cis- and trans- acting information to natural epigenetic variation. The majority of DMRs that occur in genomic regions without genetic variation are controlled by cis-acting differences and exhibit relatively stable inheritance. This study provides evidence for naturally occurring epigenetic variation in maize, including examples of pure epigenetic variation that is not conditioned by genetic differences. The epigenetic differences are variable within maize populations and exhibit relatively stable trans-generational inheritance. The detected examples of epigenetic variation, including some without tightly linked genetic variation, may contribute to complex trait variation.
Vyšlo v časopise:
Heritable Epigenetic Variation among Maize Inbreds. PLoS Genet 7(11): e32767. doi:10.1371/journal.pgen.1002372
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002372
Souhrn
Epigenetic variation describes heritable differences that are not attributable to changes in DNA sequence. There is the potential for pure epigenetic variation that occurs in the absence of any genetic change or for more complex situations that involve both genetic and epigenetic differences. Methylation of cytosine residues provides one mechanism for the inheritance of epigenetic information. A genome-wide profiling of DNA methylation in two different genotypes of Zea mays (ssp. mays), an organism with a complex genome of interspersed genes and repetitive elements, allowed the identification and characterization of examples of natural epigenetic variation. The distribution of DNA methylation was profiled using immunoprecipitation of methylated DNA followed by hybridization to a high-density tiling microarray. The comparison of the DNA methylation levels in the two genotypes, B73 and Mo17, allowed for the identification of approximately 700 differentially methylated regions (DMRs). Several of these DMRs occur in genomic regions that are apparently identical by descent in B73 and Mo17 suggesting that they may be examples of pure epigenetic variation. The methylation levels of the DMRs were further studied in a panel of near-isogenic lines to evaluate the stable inheritance of the methylation levels and to assess the contribution of cis- and trans- acting information to natural epigenetic variation. The majority of DMRs that occur in genomic regions without genetic variation are controlled by cis-acting differences and exhibit relatively stable inheritance. This study provides evidence for naturally occurring epigenetic variation in maize, including examples of pure epigenetic variation that is not conditioned by genetic differences. The epigenetic differences are variable within maize populations and exhibit relatively stable trans-generational inheritance. The detected examples of epigenetic variation, including some without tightly linked genetic variation, may contribute to complex trait variation.
Zdroje
1. BirdA 2007 Perceptions of epigenetics. Nature 447 7143 396 398
2. ChanSWHendersonIRJacobsenSE 2005 Gardening the genome: DNA methylation in arabidopsis thaliana. Nat Rev Genet 6 351 360
3. SlotkinRKMartienssenR 2007 Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 8 272 285 10.1038/nrg2072
4. RasmussonDCPhillipsRL 1997 Plant breeding progress and genetic diversity from de novo variation and elevated epistasis. Crop Sci 37 303 310
5. RichardsEJ 2006 Inherited epigenetic variation–revisiting soft inheritance. Nat Rev Genet 7 395 401
6. FeinbergAP 2007 Phenotypic plasticity and the epigenetics of human disease. Nature 447 7143 433 440
7. JirtleRLSkinnerMK 2007 Environmental epigenomics and disease susceptibility. Nat Rev Genet 8 253 262
8. VaughnMWTanurdzicMLippmanZJiangHCarrasquilloR 2007 Epigenetic natural variation in arabidopsis thaliana. PLoS Biol 5 e174 doi:10.1371/journal.pbio.0050174
9. RichardsEJ 2008 Population epigenetics. Curr Opin Genet Dev 18 221 226
10. JohannesFColotVJansenRC 2008 Epigenome dynamics: A quantitative genetics perspective. Nat Rev Genet 9 883 890
11. BucklerESGautBSMcMullenMD 2006 Molecular and functional diversity of maize. Curr Opin Plant Biol 9 172 176
12. MessingJDoonerHK 2006 Organization and variability of the maize genome. Curr Opin Plant Biol 9 157 163
13. RabinowiczPDBennetzenJL 2006 The maize genome as a model for efficient sequence analysis of large plant genomes. Curr Opin Plant Biol 9 149 156
14. SchnablePSWareDFultonRSSteinJCWeiF 2009 The B73 maize genome: Complexity, diversity, and dynamics. Science 326 5956 1112 1115
15. WeilCMartienssenR 2008 Epigenetic interactions between transposons and genes: Lessons from plants. Curr Opin Genet Dev 18 188 192
16. YuJHollandJBMcMullenMDBucklerES 2008 Genetic design and statistical power of nested association mapping in maize. Genetics 178 539 551
17. McMullenMDKresovichSVilledaHSBradburyPLiH 2009 Genetic properties of the maize nested association mapping population. Science 325 5941 737 740
18. LippmanZGendrelAVBlackMVaughnMWDedhiaN 2004 Role of transposable elements in heterochromatin and epigenetic control. Nature 430 6998 471 476
19. ZhangXYazakiJSundaresanACokusSChanSW 2006 Genome-wide high-resolution mapping and functional analysis of DNA methylation in arabidopsis. Cell 126 1189 1201
20. ZilbermanDGehringMTranRKBallingerTHenikoffS 2007 Genome-wide analysis of arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat Genet 39 61 69
21. MiuraANakamuraMInagakiSKobayashiASazeH 2009 An arabidopsis jmjC domain protein protects transcribed genes from DNA methylation at CHG sites. EMBO J 28 1078 1086
22. FengSCokusSJZhangXChenPYBostickM 2010 Conservation and divergence of methylation patterning in plants and animals. Proc Natl Acad Sci U S A 107 8689 8694
23. WangXEllingAALiXLiNPengZ 2009 Genome-wide and organ-specific landscapes of epigenetic modifications and their relationships to mRNA and small RNA transcriptomes in maize. Plant Cell 21 1053 1069
24. FinneganEJ 2002 Epialleles - a source of random variation in times of stress. Curr Opin Plant Biol 5 101 106
25. KaliszSPuruggananMD 2004 Epialleles via DNA methylation: Consequences for plant evolution. Trends Ecol Evol 19 309 314
26. LukensLNZhanS 2007 The plant genome's methylation status and response to stress: Implications for plant improvement. Curr Opin Plant Biol 10 317 322
27. RichardsEJ 2011 Natural epigenetic variation in plant species: A view from the field. Curr Opin Plant Biol 14 204 209
28. ReindersJWulffBBMirouzeMMari-OrdonezADappM 2009 Compromised stability of DNA methylation and transposon immobilization in mosaic arabidopsis epigenomes. Genes Dev 23 939 950
29. JohannesFPorcherETeixeiraFKSaliba-ColombaniVSimonM 2009 Assessing the impact of transgenerational epigenetic variation on complex traits. PLoS Genet 5 e1000530 doi:10.1371/journal.pgen.1000530
30. RouxFColome-TatcheMEdelistCWardenaarRGuercheP 2011 Genome-wide epigenetic perturbation jump-starts patterns of heritable variation found in nature. Genetics 188 1015 1017
31. JohannesFColome-TatcheM 2011 Quantitative epigenetics through epigenomic perturbation of isogenic lines. Genetics 188 215 227
32. RiddleNCRichardsEJ 2002 The control of natural variation in cytosine methylation in arabidopsis. Genetics 162 355 363
33. RiddleNCRichardsEJ 2005 Genetic variation in epigenetic inheritance of ribosomal RNA gene methylation in arabidopsis. Plant J 41 524 532
34. WooHRPontesOPikaardCSRichardsEJ 2007 VIM1, a methylcytosine-binding protein required for centromeric heterochromatinization. Genes Dev 21 267 277
35. ZhangXShiuSHCalABorevitzJO 2008 Global analysis of genetic, epigenetic and transcriptional polymorphisms in arabidopsis thaliana using whole genome tiling arrays. PL+oS Genet 4 e1000032
36. BenderJFinkGR 1995 Epigenetic control of an endogenous gene family is revealed by a novel blue fluorescent mutant of arabidopsis. Cell 83 725 734
37. JacobsenSEMeyerowitzEM 1997 Hypermethylated SUPERMAN epigenetic alleles in arabidopsis. Science 277 5329 1100 1103
38. CubasPVincentCCoenE 1999 An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401 6749 157 161
39. MorganHDSutherlandHGMartinDIWhitelawE 1999 Epigenetic inheritance at the agouti locus in the mouse. Nat Genet 23 314 318
40. ChandlerVLEgglestonWBDorweilerJE 2000 Paramutation in maize. Plant Mol Biol 43 2–3 121 145
41. StokesTLKunkelBNRichardsEJ 2002 Epigenetic variation in arabidopsis disease resistance. Genes Dev 16 171 182
42. RakyanVKChongSChampMECuthbertPCMorganHD 2003 Transgenerational inheritance of epigenetic states at the murine axin allele occurs after maternal and paternal transmission. Proc Natl Acad Sci U S A 100 2538 2543
43. SuterCMMartinDIWardRL 2004 Germline epimutation of MLH1 in individuals with multiple cancers. Nat Genet 36 497 501
44. ManningKTorMPooleMHongYThompsonAJ 2006 A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat Genet 38 948 952
45. MakarevitchIStuparRMIniguezALHaunWJBarbazukWB 2007 Natural variation for alleles under epigenetic control by the maize chromomethylase zmet2. Genetics 177 749 760
46. SlotkinRKFreelingMLischD 2005 Heritable transposon silencing initiated by a naturally occurring transposon inverted duplication. Nat Genet 37 641 644
47. Arteaga-VazquezMSidorenkoLRabanalFAShrivistavaRNobutaK 2010 RNA-mediated trans-communication can establish paramutation at the b1 locus in maize. Proc Natl Acad Sci U S A 107 12986 12991
48. HaunWJLaoueille-DupratSO'connellMJSpillaneCGrossniklausU 2007 Genomic imprinting, methylation and molecular evolution of maize enhancer of zeste (mez) homologs. Plant J 49 325 337
49. GoreMAChiaJMElshireRJSunQErsozES 2009 A first-generation haplotype map of maize. Science 326 5956 1115 1117
50. SpringerNMYingKFuYJiTYehCT 2009 Maize inbreds exhibit high levels of copy number variation (CNV) and presence/absence variation (PAV) in genome content. PLoS Genet 5 e1000734 doi:10.1371/journal.pgen.1000734
51. BeloABeattyMKHondredDFenglerKALiB 2010 Allelic genome structural variations in maize detected by array comparative genome hybridization. Theor Appl Genet 120 355 367
52. VenkatramanESOlshenAB 2007 A faster circular binary segmentation algorithm for the analysis of array CGH data. Bioinformatics 23 657 663
53. DempsterAPLairdNMRubinDB 1977 Maximum likelihood from incomplete data via the EM algorithm. Journal of the Royal Statistical Society.Series B (Methodological) 39 1 38
54. LiuSYehCTJiTYingKWuH 2009 Mu transposon insertion sites and meiotic recombination events co-localize with epigenetic marks for open chromatin across the maize genome. PLoS Genet 5 e1000733 doi:10.1371/journal.pgen.1000733
55. ListerRO'MalleyRCTonti-FilippiniJGregoryBDBerryCC 2008 Highly integrated single-base resolution maps of the epigenome in arabidopsis. Cell 133 523 536
56. LiPPonnalaLGandotraNWangLSiY 2010 The developmental dynamics of the maize leaf transcriptome. Nat Genet 42 1060 1067
57. SchnableJCSpringerNMFreelingM 2011 Differentiation of the maize subgenomes by genome dominance and both ancient and ongoing gene loss. Proc Natl Acad Sci U S A 108 4069 4074
58. EichtenSRFoersterJMde LeonNKaiYYehCT 2011 B73-Mo17 near-isogenic lines demonstrate dispersed structural variation in maize. Plant Physiol 156 1679 1690
59. ChandlerVLStamM 2004 Chromatin conversations: Mechanisms and implications of paramutation. Nat Rev Genet 5 532 544
60. SpringerNMGutierrez-MarcosJF 2009 Imprinting in maize. Anonymous Handbook of Maize Springer New York 429 440
61. FedoroffNSchlappiMRainaR 1995 Epigenetic regulation of the maize spm transposon. Bioessays 17 291 297
62. LischD 2002 Mutator transposons. Trends Plant Sci 7 498 504
63. SchnableJCFreelingM 2011 Genes identified by visible mutant phenotypes show increased bias toward one of two subgenomes of maize. PLoS ONE 6 e17855 doi:10.1371/journal.pone.0017855
64. HanseyCNJohnsonJMSekhonRSKaepplerSMLeonNd 2011 Genetic diversity of a maize association population with restricted phenology. Crop Sci 51 704 715
65. Swanson-WagnerRAEichtenSRKumariSTiffinPSteinJC 2010 Pervasive gene content variation and copy number variation in maize and its undomesticated progenitor. Genome Res 20 1689 1699
66. HaunWJSpringerNM 2008 Maternal and paternal alleles exhibit differential histone methylation and acetylation at maize imprinted genes. Plant J 56 903 912
67. SmythGK 2004 Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3 Article3
68. FraleyCRafteryAE 2006 MCLUST version 3 for R: Normal mixture modeling and model-based clustering. Department of Statistics: University of Washington
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2011 Číslo 11
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