Genetic sources of population epigenomic variation

Nature Reviews Genetics

Volumn 17, Issue 6, 2016, Pages 319-332

  Taudt, Aaron ^a   Colomé Tatché, Maria ^a,b   Johannes, Frank ^a,c  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOSINE; DINUCLEOTIDE; DNA; HISTONE H2A; HISTONE H2B; HISTONE H3; HISTONE H4; INCYCLINIDE; SMALL INTERFERING RNA;

CELL DIFFERENTIATION; CHROMATIN; CPG ISLAND; DNA METHYLATION; DNA PACKAGING; ENHANCER REGION; ENVIRONMENTAL EXPOSURE; EPIGENETICS; GENE EXPRESSION; GENETIC ASSOCIATION; GENETIC POLYMORPHISM; GENETIC VARIATION; GENOME-WIDE ASSOCIATION STUDY; HISTONE MODIFICATION; HUMAN; INHERITANCE; NEXT GENERATION SEQUENCING; PHENOTYPE; POPULATION GENETICS; PRIORITY JOURNAL; PROMOTER REGION; QUANTITATIVE TRAIT LOCUS; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM; TRANSPOSON; GENETIC EPIGENESIS; GENETICS; MOLECULAR EVOLUTION; PROCEDURES;

EPIGENESIS, GENETIC; EPIGENOMICS; EVOLUTION, MOLECULAR; GENETIC VARIATION; GENETICS, POPULATION; HUMANS; PHENOTYPE;

EID: 84966470585     PISSN: 14710056     EISSN: 14710064     Source Type: Journal    
DOI: 10.1038/nrg.2016.45     Document Type: Review

References (140)

1. Park, P. ChIP-seq: advantages and challenges of a maturing technology. Nat. Rev. Genet. 10, 669-680 (2009).
2. Laird, P. W. Principles and challenges of genome-wide DNA methylation analysis. Nat. Rev. Genet. 11, 191-203 (2010).
3. Adams, D., et al. BLUEPRINT to decode the epigenetic signature written in blood. Nat. Biotechnol. 30, 224-226 (2012).
4. Bernstein, B. E., et al. The NIH Roadmap Epigenomics Mapping Consortium. Nat. Biotechnol. 28, 1045-1048 (2010).
5. Kundaje, A., et al. Integrative analysis of 111 reference human epigenomes. Nature 518, 317-330 (2015).
6. Ernst, J., & Kellis, M. Discovery and characterization of chromatin states for systematic annotation of the human genome. Nat. Biotechnol. 28, 817-825 (2010).
7. Kasowski, M., et al. Extensive variation in chromatin states across humans. Science 342, 750-752 (2013).
8. Rakyan, V. K., Down, T. A., Balding, D. J., & Beck, S. Epigenome-wide association studies for common human diseases. Nat. Rev. Genet. 12, 529-541 (2011).
9. Mill, J., & Heijmans, B. T. From promises to practical strategies in epigenetic epidemiology. Nat. Rev. Genet. 14, 585-594 (2013).
10. Zhou, V. W., Goren, A., & Bernstein, B. E. Charting histone modifications and the functional organization of mammalian genomes. Nat. Rev. Genet. 12, 7-18 (2011).
11. Kouzarides, T. Chromatin modifications and their function. Cell 128, 693-705 (2007).
12. Bernstein, B. E., Meissner, A., & Lander, E. S. The mammalian epigenome. Cell 128, 669-681 (2007).
13. Strahl, B. D., & Allis, C. D. The language of covalent histone modifications. Nature 403, 41-45 (2000).
14. Jenuwein, T., & Allis, C. D. Translating the histone code. Science 293, 1074-1080 (2001).
15. Li, X., et al. High-resolution mapping of epigenetic modifications of the rice genome uncovers interplay between DNA methylation, histone methylation, and gene expression. Plant Cell 20, 259-276 (2008).
16. Hon, G., Ren, B., & Wang, W. ChromaSig: a probabilistic approach to finding common chromatin signatures in the human genome. PLoS Comput. Biol. 4, e1000201 (2008).
17. Wang, Z., et al. Combinatorial patterns of histone acetylations and methylations in the human genome. Nat. Genet. 40, 897-903 (2008).
18. Hon, G., Wang, W., & Ren, B. Discovery and annotation of functional chromatin signatures in the human genome. PLoS Comput. Biol. 5, e1000566 (2009).
19. Roy, S., et al. Identification of functional elements and regulatory circuits by Drosophila modENCODE. Science 330, 1787-1797 (2010).
20. Kharchenko, P. V., et al. Comprehensive analysis of the chromatin landscape in Drosophila melanogaster. Nature 471, 480-485 (2011).
21. Riddle, N. C., et al. Plasticity in patterns of histone modifications and chromosomal proteins in Drosophila heterochromatin. Genome Res. 21, 147-163 (2010).
22. Gerstein, M. B., et al. Integrative analysis of the Caenorhabditis elegans genome by the modENCODE project. Science 330, 1775-1787 (2010).
23. Filion, G. J., et al. Systematic protein location mapping reveals five principal chromatin types in Drosophila cells. Cell 143, 212-224 (2010).
24. Roudier, F., et al. Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. EMBO J. 30, 1928-1938 (2011).
25. Liu, T., et al. Broad chromosomal domains of histone modification patterns in C. elegans. Genome Res. 21, 227-236 (2011).
26. Hoffman, M. M., et al. Unsupervised pattern discovery in human chromatin structure through genomic segmentation. Nat. Methods 9, 473-476 (2012).
27. Lai, W. K. M., & Buck, M. J. An integrative approach to understanding the combinatorial histone code at functional elements. Bioinformatics 29, 2231-2237 (2013).
28. Luo, C., et al. Integrative analysis of chromatin states in Arabidopsis identified potential regulatory mechanisms for natural antisense transcript production. Plant J. 73, 77-90 (2013).
29. Sequeira-Mendes, J., et al. The functional topography of the Arabidopsis genome is organized in a reduced number of linear motifs of chromatin states. Plant Cell 26, 2351-2366 (2014).
30. Baker, K., et al. Chromatin state analysis of the barley epigenome reveals a higher-order structure defined by H3K27me1 and H3K27me3 abundance. Plant J. 84, 111-124 (2015).
31. Taudt, A. Nguyen, M. A., Heinig, M., Johannes, F., & Colome-Tatche, M. chromstaR: Tracking combinatorial chromatin state dynamics in space and time. bioRxiv http://dx.doi.org/10.1101/038612 (2016).
32. Lara-Astiaso, D., et al. Chromatin state dynamics during blood formation. Science 55, 1-10 (2014).
33. Leung, D., et al. Integrative analysis of haplotype-resolved epigenomes across human tissues. Nature 518, 350-354 (2015).
34. Andersson, R. Promoter or enhancer, what's the difference? Deconstruction of established distinctions and presentation of a unifying model. Bioessays 37, 314-323 (2015).
35. Degner, J. F., et al. DNaseI sensitivity QTLs are a major determinant of human expression variation. Nature 482, 390-394 (2012).
36. Kilpinen, H., et al. Coordinated effects of sequence variation on DNA binding, chromatin structure, and transcription. Science 342, 744-747 (2013).
37. McVicker, G., et al. Identification of genetic variants that affect histone modifications in human cells. Science 342, 747-749 (2013).
38. Waszak, S., et al. Population variation and genetic control of modular chromatin architecture in humans. Cell 162, 1039-1050 (2015).
39. Grubert, F., et al. Genetic control of chromatin states in humans involves local and distal chromosomal interactions. Cell 162, 1051-1065 (2015).
40. Kimura, H. Histone modifications for human epigenome analysis. J. Hum. Genet. 58, 439-445 (2013).
41. Dixon, J. R., et al. Chromatin architecture reorganization during stem cell differentiation. Nature 518, 331-336 (2015).
42. Banovich, N. E., et al. Methylation QTLs are associated with coordinated changes in transcription factor binding, histone modifications, and gene expression levels. PLoS Genet. 10, e1004663 (2014).
43. Stadler, M. B., et al. DNA-binding factors shape the mouse methylome at distal regulatory regions. Nature 480, 490-495 (2011).
44. Esteller, M. Cancer epigenomics: DNA methylomes and histone-modification maps. Nat. Rev. Genet. 8, 286-298 (2007).
45. Rintisch, C., et al. Natural variation of histone modification and its impact on gene expression in the rat genome. Genome Res. 24, 942-953 (2014).
46. Wysocka, J., et al. WDR5 associates with histone H3 methylated at K4 and is essential for H3 K4 methylation and vertebrate development. Cell 121, 859-872 (2005).
47. Lee, K., et al. Genetic landscape of open chromatin in yeast. PLoS Genet. 9, e1003229 (2013).
48. Chai, X., Nagarajan, S., Kim, K., Lee, K., & Choi, J. K. Regulation of the boundaries of accessible chromatin. PLoS Genet. 9, e1003778 (2013).
49. McDaniell, R., et al. Heritable individual-specific and allele-specific chromatin signatures in humans. Science 328, 235-239 (2010).
50. Feng, S., et al. Conservation and divergence of methylation patterning in plants and animals. Proc. Natl Acad. Sci. USA 107, 8689-8694 (2010).
51. Zemach, A., McDaniel, I. E., Silva, P., & Zilberman, D. Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science 328, 916-919 (2010).
52. Law, J. A., & Jacobsen, S. E. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet. 11, 204-220 (2010).
53. Smith, Z. D., & Meissner, A. DNA methylation: roles in mammalian development. Nat. Rev. Genet. 14, 204-220 (2013).
54. Ziller, M. J., et al. Charting a dynamic DNA methylation landscape of the human genome. Nature 500, 477-481 (2013).
55. Gifford, C. A., et al. Transcriptional and epigenetic dynamics during specification of human embryonic stem cells. Cell 153, 1149-1163 (2013).
56. Cedar, H., & Bergman, Y. Linking DNA methylation and histone modification: patterns and paradigms. Nat. Rev. Genet. 10, 295-304 (2009).
57. Du, J., Johnson, L. M., Jacobsen, S. E., & Patel, D. J. DNA methylation pathways and their crosstalk with histone methylation. Nat. Rev. Mol. Cell. Biol. 16, 519-532 (2015).
58. Michels, K. B., et al. Recommendations for the design and analysis of epigenome-wide association studies. Nat. Methods 10, 949-955 (2013).
59. Dedeurwaerder, S., et al. Evaluation of the Infinium Methylation 450K technology. Epigenomics 3, 771-784 (2011).
60. McRae, A. F., et al. Contribution of genetic variation to transgenerational inheritance of DNA methylation. Genome Biol. 15, R73 (2014).
61. Bell, J. T., et al. Epigenome-wide scans identify differentially methylated regions for age and age-related phenotypes in a healthy ageing population. PLoS Genet. 8, e1002629 (2012).
62. Gordon, L., et al. Neonatal DNA methylation profile in human twins is specified by a complex interplay between intrauterine environmental and genetic factors, subject to tissue-specific influence. Genome Res. 22, 1395-1406 (2012).
63. Wright, F. A., et al. Heritability and genomics of gene expression in peripheral blood. Nat. Genet. 46, 430-437 (2014).
64. Carja, O., et al. Worldwide patterns of human epigenetic variation. bioRxiv http://dx.doi.org/ 10.1101/021931 (2015).
65. Gibbs, J. R., et al. Abundant quantitative trait loci exist for DNA methylation and gene expression in human brain. PLoS Genet. 6, e1000952 (2010).
66. Zhang, D., et al. Genetic control of individual differences in gene-specific methylation in human brain. Am. J. Hum. Genet. 86, 411-419 (2010).
67. Bell, J. T., et al. DNA methylation patterns associate with genetic and gene expression variation in HapMap cell lines. Genome Biol. 12, R10 (2011).
68. Fraser, H. B., Lam, L. L., Neumann, S. M., & Kobor, M. S. Population-specificity of human DNA methylation. Genome Biol. 13, R8 (2012).
69. van Eijk, K. R., et al. Genetic analysis of DNA methylation and gene expression levels in whole blood of healthy human subjects. BMC Genomics 13, 636 (2012).
70. Moen, E. L., et al. Genome-wide variation of cytosine modifications between European and African populations and the implications for complex traits. Genetics 194, 987-996 (2013).
71. Gutierrez-Arcelus, M., et al. Passive and active DNA methylation and the interplay with genetic variation in gene regulation. eLife 2, e00523 (2013).
72. Olsson, A. H., et al. Genome-wide associations between genetic and epigenetic variation influence mRNA expression and insulin secretion in human pancreatic islets. PLoS Genet. 10, e1004735 (2014).
73. Wagner, J. R., et al. The relationship between DNA methylation, genetic and expression inter-individual variation in untransformed human fibroblasts. Genome Biol. 15, R37 (2014).
74. Zhang, X., et al. Linking the genetic architecture of cytosine modifications with human complex traits. Hum. Mol. Genet. 23, 5893-5905 (2014).
75. McClay, J. L., et al. High density methylation QTL analysis in human blood via next-generation sequencing of the methylated genomic DNA fraction. Genome Biol. 16, 291 (2015).
76. Busche, S., et al. Population whole-genome bisulfite sequencing across two tissues highlights the environment as the principal source of human methylome variation. Genome Biol. 16, 290 (2015).
77. Morris, T. J., & Beck, S. Analysis pipelines and packages for Infinium HumanMethylation450 BeadChip (450k) data. Methods 72, 3-8 (2015).
78. Moran, S., Arribas, C., & Esteller, M. Validation of a DNA methylation microarray for 850, 000 CpG sites of the human genome enriched in enhancer sequences. Epigenomics (2015).
79. Shoemaker, R., Deng, J., Wang, W., & Zhang, K. Allele-specific methylation is prevalent and is contributed by CpG-SNPs in the human genome. Genome Res. 20, 883-889 (2010).
80. Domcke, S., et al. Competition between DNA methylation and transcription factors determines binding of NRF1. Nature 528, 575-579 (2015).
81. Schmitz, R. J., et al. Patterns of population epigenomic diversity. Nature 495, 193-198 (2013).
82. Dubin, M. J., et al. DNA methylation in Arabidopsis has a genetic basis and shows evidence of local adaptation. eLife 4, e05255 (2015).
83. Eichten, S. R., et al. Epigenetic and genetic influences on DNA methylation variation in maize populations. Plant Cell 25, 2783-2797 (2013).
84. Schmitz, R. J., et al. Epigenome-wide inheritance of cytosine methylation variants in a recombinant inbred population. Genome Res. 23, 1663-1674 (2013).
85. Alonso, C., Perez, R., Bazaga, P., & Herrera, C. M. Global DNA cytosine methylation as an evolving trait: phylogenetic signal and correlated evolution with genome size in angiosperms. Front. Genet. 6, 4 (2015).
86. Seymour, D. K., Koenig, D., Hagmann, J., Becker, C., & Weigel, D. Evolution of DNA methylation patterns in the Brassicaceae is driven by differences in genome organization. PLoS Genet. 10, e1004785 (2014).
87. Regulski, M., et al. The maize methylome influences mRNA splice sites and reveals widespread paramutation-like switches guided by small RNA. Genome Res. 23, 1651-1662 (2013).
88. Vaughn, M. W., et al. Epigenetic natural variation in Arabidopsis thaliana. PLoS Biol. 5, 1617-1629 (2007).
89. Shen, H., et al. Genome-wide analysis of DNA methylation and gene expression changes in two Arabidopsis ecotypes and their reciprocal hybrids. Plant Cell 24, 875-892 (2012).
90. Hagmann, J., et al. Century-scale methylome stability in a recently diverged Arabidopsis thaliana lineage. PLoS Genet. 11, e1004920 (2015).
91. Schmitz, R. J., & Ecker, J. R. Epigenetic and epigenomic variation in Arabidopsis thaliana. Trends Plant Sci. 17, 149-154 (2012).
92. Becker, C., & Weigel, D. Epigenetic variation: origin and transgenerational inheritance. Curr. Opin. Plant Biol. 15, 562-567 (2012).
93. van der Graaf, A., et al. Rate, spectrum, and evolutionary dynamics of spontaneous epimutations. Proc. Natl Acad. Sci. USA 6676-6681 (2015).
94. Pecinka, A., Abdelsamad, A., & Vu, G. T. H. Hidden genetic nature of epigenetic natural variation in plants. Trends Plant Sci. 18, 625-632 (2013).
95. Fujimoto, R., et al. Molecular mechanisms of epigenetic variation in plants. Int. J. Mol. Sci. 13, 9900-9922 (2012).
96. Hollister, J. D., & Gaut, B. S. Epigenetic silencing of transposable elements: a trade-off between reduced transposition and deleterious effects on neighboring gene expression. Genome Res. 19, 1419-1428 (2009).
97. Bennetzen, J. L., & Wang, H. The contributions of transposable elements to the structure, function, and evolution of plant genomes. Annu. Rev. Plant Biol. 65, 505-530 (2014).
98. Stroud, H., Greenberg, M. V. C., Feng, S., Bernatavichute, Y. V., & Jacobsen, S. E. Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell 152, 352-364 (2013).
99. Li, Q., et al. Genetic perturbation of the maize methylome. Plant Cell 26, 4602-4616 (2014).
100. Shen, X., et al. Natural CMT2 variation is associated with genome-wide methylation changes and temperature seasonality. PLoS Genet. 10, e1004842 (2014).
101. Lindroth, A. M., et al. Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science 292, 2077-2080 (2001).
102. Takuno, S., & Gaut, B. S. Body-methylated genes in Arabidopsis thaliana are functionally important and evolve slowly. Mol. Biol. Evol. 29, 219-227 (2012).
103. Takuno, S., & Gaut, B. S. Gene body methylation is conserved between plant orthologs and is of evolutionary consequence. Proc. Natl Acad. Sci. USA 110, 1797-1802 (2013).
104. Takuno, S., Ran, J. H., & Gaut, B. S. Evolutionary patterns of genic DNA methylation vary across land plants. Nat. Plants 2, 15222 (2016).
105. Long, Q., et al. Massive genomic variation and strong selection in Arabidopsis thaliana lines from Sweden. Nat. Genet. 45, 884-890 (2013).
106. Johannes, F., Colot, V., & Jansen, R. C. Epigenome dynamics: a quantitative genetics perspective. Nat. Rev. Genet. 9, 883-890 (2008).
107. Becker, C., et al. Spontaneous epigenetic variation in the Arabidopsis thaliana methylome. Nature 480, 245-249 (2011).
108. Schmitz, R. J., et al. Transgenerational epigenetic instability is a source of novel methylation variants. Science 334, 369-373 (2011).
109. Jiang, C., et al. Environmentally responsive genome-wide accumulation of de novo Arabidopsis thaliana mutations and epimutations. Genome Res. 24, 1821-1829 (2014).
110. Ossowski, S., et al. The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science 327, 92-94 (2010).
111. Virdi, K. S., et al. Arabidopsis MSH1 mutation alters the epigenome and produces heritable changes in plant growth. Nat. Commun. 6, 6386 (2015).
112. Eichten, S. R., et al. Heritable epigenetic variation among maize inbreds. PLoS Genet. 7, e1002372 (2011).
113. Amoah, S., et al. A hypomethylated population of Brassica rapa for forward and reverse epi-genetics. BMC Plant Biol. 12, 193 (2012).
114. Hauben, M., et al. Energy use efficiency is characterized by an epigenetic component that can be directed through artificial selection to increase yield. Proc. Natl Acad. Sci. USA 106, 20109-20114 (2009).
115. Bossdorf, O., Arcuri, D., Richards, C. L., & Pigliucci, M. Experimental alteration of DNA methylation affects the phenotypic plasticity of ecologically relevant traits in Arabidopsis thaliana. Evol. Ecol. 24, 541-553 (2010).
116. Li, Q., Eichten, S. R., Hermanson, P. J., & Springer, N. M. Inheritance patterns and stability of DNA methylation variation in maize near-isogenic lines. Genetics 196, 667-676 (2014).
117. Cortijo, S., et al. Mapping the epigenetic basis of complex traits. Science 343, 1145-1148 (2014).
118. Verhoeven, K. J. F., Jansen, J. J., van Dijk, P. J., & Biere, A. Stress-induced DNA methylation changes and their heritability in asexual dandelions. New Phytol. 185, 1108-1118 (2010).
119. Reinders, J., et al. Compromised stability of DNA methylation and transposon immobilization in mosaic Arabidopsis epigenomes. Genes Dev. 23, 939-950 (2009).
120. Johannes, F., et al. Assessing the impact of transgenerational epigenetic variation on complex traits. PLoS Genet. 5, e1000530 (2009).
121. Roux, F., et al. Genome-wide epigenetic perturbation jump-starts patterns of heritable variation found in nature. Genetics 188, 1015-1017 (2011).
122. Zhang, Y. Y., Fischer, M., Colot, V., & Bossdorf, O. Epigenetic variation creates potential for evolution of plant phenotypic plasticity. New Phytol. 197, 314-322 (2013).
123. Slatkin, M. Epigenetic inheritance and the missing heritability problem. Genetics 182, 845-850 (2009).
124. Johannes, F., & Colome-Tatche, M. Quantitative epigenetics through epigenomic perturbation of isogenic lines. Genetics 188, 215-227 (2011).
125. Day, T., & Bonduriansky, R. A unified approach to the evolutionary consequences of genetic and nongenetic inheritance. Am. Nat. 178, E18-E36 (2011).
126. Geoghegan, J. L., & Spencer, H. G. Population-epigenetic models of selection. Theor. Popul. Biol. 81, 232-242 (2012).
127. Klironomos, F. D., Berg, J., & Collins, S. How epigenetic mutations can affect genetic evolution: model and mechanism. Bioessays 35, 571-578 (2013).
128. Furrow, R. E. Epigenetic inheritance, epimutation, and the response to selection. PLoS ONE 9, e101559 (2014).
129. Furrow, R. E., & Feldman, M. W. Genetic variation and the evolution of epigenetic regulation. Evolution 68, 673-683 (2014).
130. Charlesworth, B., & Jain, K. Purifying selection, drift, and reversible mutation with arbitrarily high mutation rates. Genetics 198, 1587-1602 (2014).
131. Kronholm, I., & Collins, S. Epigenetic mutations can both help and hinder adaptive evolution. Mol. Ecol. 25, 1856-1868 (2015).
132. Wang, J., & Fan, C. A neutrality test for detecting selection on DNA methylation using single methylation polymorphism frequency spectrum. Genome Biol. Evol. 7, 154-171 (2015).
133. Zilberman, D., Coleman-Derr, D., Ballinger, T., & Henikoff, S. Histone H2A.Z and DNA methylation are mutually antagonistic chromatin marks. Nature 456, 125-129 (2008).
134. Jackson, J. P., et al. Dimethylation of histone H3 lysine 9 is a critical mark for DNA methylation and gene silencing in Arabidopsis thaliana. Chromosoma 112, 308-315 (2004).
135. Bernatavichute, Y. V., Zhang, X., Cokus, S., Pellegrini, M., & Jacobsen, S. E. Genomewide association of histone H3 lysine nine methylation with CHG DNA methylation in Arabidopsis thaliana. PLoS ONE 3, e3156 (2008).
136. Lane, A. K., Niederhuth, C. E., Ji, L., & Schmitz, R. J. pENCODE: a plant encyclopedia of DNA elements. Annu. Rev. Genet. 48, 49-70 (2014).
137. Zeng, X., et al. jMOSAiCS: joint analysis of multiple ChIP-seq datasets. Genome Biol. 14, R38 (2013).
138. Won, K. J., et al. Comparative annotation of functional regions in the human genome using epigenomic data. Nucleic Acids Res. 41, 4423-4432 (2013).
139. Fraga, M. F., et al. Epigenetic differences arise during the lifetime of monozygotic twins. Proc. Natl Acad. Sci. USA 102, 10604-10609 (2005).
140. Schwartzman, O., & Tanay, A. Single-cell epigenomics: techniques and emerging applications. Nat. Rev. Genet. 16, 716-726 (2015).