Methylome evolution in plants

Genome Biology

Volumn 17, Issue 1, 2016, Pages

  Vidalis, Amaryllis ^a   Živković, Daniel ^a   Wardenaar, René ^b   Roquis, David ^a   Tellier, Aurélien ^a   Johannes, Frank ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

DRAWING; EPIGENETICS; METHYLATION; NATURAL POPULATION; ARABIDOPSIS; DNA METHYLATION; GENE EXPRESSION REGULATION; GENETIC VARIATION; GENETICS; MOLECULAR EVOLUTION; PLANT GENOME;

ARABIDOPSIS; DNA METHYLATION; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, PLANT; GENETIC VARIATION; GENOME, PLANT;

EID: 85006822942     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/s13059-016-1127-5     Document Type: Review

References (128)

1. Feng S. Epigenetic reprogramming in plant and animal development. Science. 2010;330:622-7.
2. Zemach A, McDaniel IE, Silva P, Zilberman D. Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science. 2010;328:916-9.
3. Niederhuth CE, Bewick AJ, Ji L, Alabady MS, Kim KD, Li Q, et al. Widespread natural variation of DNA methylation within angiosperms. Genome Biol. 2016;17:194.
4. Takuno S, Ran J-H, Gaut BS. Evolutionary patterns of genic DNA methylation vary across land plants. Nat Plants. 2016;2:15222.
5. Das OP, Messing J. Variegated phenotype and developmental methylation changes of a maize allele originating from epimutation. Genetics. 1994;136:1121-41.
6. Bender J, Fink GR. Epigenetic control of an endogenous gene family is revealed by a novel blue fluorescent mutant of Arabidopsis. Cell. 1995;83:725-34.
7. Melquist S, Bender J. Transcription from an upstream promoter controls methylation signaling from an inverted repeat of endogenous genes in Arabidopsis. Genes Dev. 2003;17:2036-47.
8. Ong-Abdullah M, Ordway JM, Jiang N, Ooi S-E, Kok S, Sarpan N, et al. Loss of Karma transposon methylation underlies the mantled somaclonal variant of oil palm. Nature. 2015;525:533-7.
9. Banks JA, Masson P, Fedoroff N. Molecular mechanisms in the developmental regulation of the maize Suppressor-Mutator transposable element. Genes Dev. 1988;2:1364-80.
10. Jacobsen SE. Hypermethylated SUPERMAN epigenetic alleles in Arabidopsis. Science. 1997;277:1100-3.
11. Soppe WJJ, Jacobsen SE, Alonso-Blanco C, Jackson JP, Kakutani T, Koornneef M, et al. The late flowering phenotype of fwa mutants is caused by gain-of-function epigenetic alleles of a homeodomain gene. Mol Cell. 2000;6:791-802.
12. Stam M, Belele C, Dorweiler JE, Chandler VL. Differential chromatin structure within a tandem array 100kb upstream of the maize b1 locus is associated with paramutation. Genes Dev. 2002;16:1906-18.
13. Colot V, Maloisel L, Rossignol JL. Interchromosomal transfer of epigenetic states in Ascobolus: transfer of DNA methylation is mechanistically related to homologous recombination. Cell. 1996;86:855-64.
14. Stokes TL, Kunkel BN, Richards EJ. Epigenetic variation in Arabidopsis disease resistance. Genes Dev. 2002;16:171-82.
15. Quadrana L, Almeida J, Asis R, Duffy T, Dominguez PG, Bermúdez L, et al. Natural occurring epialleles determine vitamin E accumulation in tomato fruits. Nat Commun. 2014;5:3027.
16. Reinders J, Wulff BBH, Mirouze M, Mari-Ordóñez A, Dapp M, Rozhon W, et al. Compromised stability of DNA methylation and transposon immobilization in mosaic Arabidopsis epigenomes. Genes Dev. 2009;23:939-50.
17. Johannes F, Porcher E, Teixeira FK, Saliba-Colombani V, Simon M, Agier N, et al. Assessing the impact of transgenerational epigenetic variation on complex traits. PLoS Genet. 2009;5:e1000530.
18. Roux F, Colomé-Tatché M, Edelist C, Wardenaar R, Guerche P, Hospital F, et al. Genome-wide epigenetic perturbation jump-starts patterns of heritable variation found in nature. Genetics. 2011;188:1015-7.
19. Eichten SR, Schmitz RJ, Springer NM. Epigenetics: beyond chromatin modifications and complex genetic regulation. Plant Physiol. 2014;165:933-47.
20. Silveira AB, Trontin C, Cortijo S, Barau J, Del Bem LEV, Loudet O, et al. Extensive natural epigenetic variation at a de novo originated gene. PLoS Genet. 2013;9:3-10.
21. Tsukahara S, Kobayashi A, Kawabe A, Mathieu O, Miura A, Kakutani T. Bursts of retrotransposition reproduced in Arabidopsis. Nature. 2009;461:423-6.
22. Mirouze M, Reinders J, Bucher E, Nishimura T, Schneeberger K, Ossowski S, et al. Selective epigenetic control of retrotransposition in Arabidopsis. Nature. 2009;461:1-5.
23. Miura A, Yonebayashi S, Watanabe K, Toyama T, Shimada H, Kakutani T. Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis. Nature. 2001;411:212-4.
24. Singer T, Yordan C, Martienssen RA. Robertson's Mutator transposons in A. thaliana are regulated by the chromatin-remodeling gene Decrease in DNA Methylation (DDM1). Genes Dev. 2001;15:591-602.
25. Cheng C, Tarutani Y, Miyao A, Ito T, Yamazaki M, Sakai H, et al. Loss of function mutations in the rice chromomethylase OsCMT3a cause a burst of transposition. Plant J. 2015;83:1069-81.
26. Kim KD, El Baidouri M, Abernathy B, Iwata-Otsubo A, Chavarro C, Gonzales M, et al. A comparative epigenomic analysis of polyploidy-derived genes in soybean and common bean. Plant Physiol. 2015;168:1433-47.
27. Maloisel L, Rossignol JL. Suppression of crossing-over by DNA methylation in Ascobolus. Genes Dev. 1998;12:1381-9.
28. Mirouze M, Lieberman-Lazarovich M, Aversano R, Bucher E, Nicolet J, Reinders J, et al. Loss of DNA methylation affects the recombination landscape in Arabidopsis. Proc Natl Acad Sci U S A. 2012;109:5880-5.
29. Colomé-Tatché M, Cortijo S, Wardenaar R, Morgado L, Lahouze B, Sarazin A, et al. Features of the Arabidopsis recombination landscape resulting from the combined loss of sequence variation and DNA methylation. Proc Natl Acad Sci U S A. 2012;109:16240-5.
30. Melamed-Bessudo C, Levy AA. Deficiency in DNA methylation increases meiotic crossover rates in euchromatic but not in heterochromatic regions in Arabidopsis. Proc Natl Acad Sci U S A. 2012;109:E981-8.
31. Yelina NE, Choi K, Chelysheva L, Macaulay M, de Snoo B, Wijnker E, et al. Epigenetic remodeling of meiotic crossover frequency in Arabidopsis thaliana DNA methyltransferase mutants. PLoS Genet. 2012;8:e1002844.
32. Shen H, He H, Li J, Chen W, Wang X, Guo L, et al. Genome-wide analysis of DNA methylation and gene expression changes in two Arabidopsis ecotypes and their reciprocal hybrids. Plant Cell. 2012;24:875-92.
33. Dapp M, Reinders J, Bédiée A, Balsera C, Bucher E, Theiler G, et al. Heterosis and inbreeding depression of epigenetic Arabidopsis hybrids. Nat Plants. 2015;1:15092.
34. Rigal M, Becker C, Pélissier T, Pogorelcnik R, Devos J, Ikeda Y, et al. Epigenome confrontation triggers immediate reprogramming of DNA methylation and transposon silencing in Arabidopsis thaliana F1 epihybrids. Proc Natl Acad Sci U S A. 2016;113:E2083-92.
35. Lauss K, Wardenaar R, van Hulten MHA, Guryev V, Keurentjes JJB, Stam M, et al. Epigenetic divergence is sufficient to trigger heterosis in Arabidopsis thaliana. bioRxiv. 2016; doi: http://dx.doi.org/10.1101/059980.
36. Groszmann M, Greaves IK, Fujimoto R, Peacock WJ, Dennis ES. The role of epigenetics in hybrid vigour. Trends Genet. 2013;29:684-90.
37. Chen ZJ. Genomic and epigenetic insights into the molecular bases of heterosis. Nat Rev Genet. 2013;14:471-82.
38. Kirkbride RC, Yu HH, Nah G, Zhang C, Shi X, Chen ZJ. An epigenetic role for disrupted paternal gene expression in postzygotic seed abortion in Arabidopsis interspecific hybrids. Mol Plant. 2015;8:1766-75.
39. Fort A, Ryder P, Mckeown PC, Wijnen C, Aarts MG, Sulpice R, et al. Disaggregating polyploidy, parental genome dosage and hybridity contributions to heterosis in Arabidopsis thaliana. New Phytol. 2016;209:590-9.
40. Groszmann M, Gonzalez-Bayon R, Lyons RL, Greaves IK, Kazan K, Peacock WJ, et al. Hormone-regulated defense and stress response networks contribute to heterosis in Arabidopsis F1 hybrids. Proc Natl Acad Sci U S A. 2015;112:E6397-406.
41. Secco D, Wang C, Shou H, Schultz MD, Chiarenza S, Nussaume L, et al. Stress induced gene expression drives transient DNA methylation changes at adjacent repetitive elements. Elife. 2015;4:e09343.
42. Feil R, Fraga MF. Epigenetics and the environment: emerging patterns and implications. Nat Rev Genet. 2012;13:97-109.
43. Meyer P. Epigenetic variation and environmental change. J Exp Bot. 2015;66:3541-8.
44. Zhang X. Dynamic differential methylation facilitates pathogen stress response in Arabidopsis. Proc Natl Acad Sci U S A. 2012;109:12842-3.
45. Yu A, Lepere G, Jay F, Wang J, Bapaume L, Wang Y, et al. Dynamics and biological relevance of DNA demethylation in Arabidopsis antibacterial defense. Proc Natl Acad Sci U S A. 2013;110:2389-94.
46. López Sánchez A, Stassen JH, Furci L, Smith LM, Ton J. The role of DNA (de)methylation in immune responsiveness of Arabidopsis. Plant J. 2016;88:361-74.
47. Espinas NA, Saze H, Saijo Y. Epigenetic control of defense signaling and priming in plants. Front Plant Sci. 2016;7:1201.
48. Luna E, Ton J. The epigenetic machinery controlling transgenerational systemic acquired resistance. Plant Signal Behav. 2012;7:615-8.
49. Conrath U, Beckers GJM, Langenbach CJG, Jaskiewicz MR. Priming for enhanced defense. Annu Rev Phytopathol. 2015;53:97-119.
50. Rapp RA, Wendel JF. Epigenetics and plant evolution. New Phytol. 2005;168:81-91.
51. Richards EJ, Reinders J, Wulff BBH, Mirouze M. Quantitative epigenetics: DNA sequence variation need not apply. Genes Dev. 2009;23:1601-5.
52. Weigel D, Colot V. Epialleles in plant evolution. Genome Biol. 2012;13:249.
53. Diez CM, Roessler K, Gaut BS. Epigenetics and plant genome evolution. Curr Opin Plant Biol. 2014;18:1-8.
54. Springer NM. Epigenetics and crop improvement. Trends Genet. 2013;29:241-7.
55. Ji L, Neumann DA, Schmitz RJ. Crop epigenomics: identifying, unlocking, and harnessing cryptic variation in crop genomes. Mol Plant. 2014;8:860-70.
56. Law JA, Jacobsen SE. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet. 2010;11:204-20.
57. Stroud H, Greenberg MVC, Feng S, Bernatavichute YV, Jacobsen SE. Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell. 2013;152:352-64.
58. Laird PW. Principles and challenges of genome-wide DNA methylation analysis. Nat Rev Genet. 2010;11:191-203.
59. Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan SWL, Chen H, et al. Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell. 2006;126:1189-201.
60. Cokus SJ, Feng S, Zhang X, Chen Z, Merriman B, Haudenschild CD, et al. Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature. 2008;452:215-9.
61. Lister R, Malley RCO, Tonti-filippini J, Gregory BD, Berry CC, Miller AH, et al. Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell. 2008;133:523-36.
62. Zilberman D, Gehring M, Tran RK, Ballinger T, Henikoff S. Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat Genet. 2007;39:61-9.
63. Schmitz RJ, Schultz MD, Urich MA, Nery JR, Pelizzola M, Libiger O, et al. Patterns of population epigenomic diversity. Nature. 2013;495:193-8.
64. Gent JI, Ellis NA, Guo L, Harkess AE, Yao Y, Zhang X, et al. CHH islands: de novo DNA methylation in near-gene chromatin regulation in maize. Genome Res. 2013;23:628-37.
65. Seymour DK, 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. 2014;10:e1004785.
66. Amborella Genome Project, Albert VA, Barbazuk WB, dePamphilis CW, Der JP, Leebens-Mack J, et al. The Amborella genome and the evolution of flowering plants. Science. 2013;342:1241089.
67. Zhong S, Fei Z, Chen Y-R, Zheng Y, Huang M, Vrebalov J, et al. Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening. Nat Biotechnol. 2013;31:154-9.
68. Alonso C, Pérez R, Bazaga P, Herrera CM. Global DNA cytosine methylation as an evolving trait: phylogenetic signal and correlated evolution with genome size in angiosperms. Front Genet. 2015;5:1-9.
69. Cao J, Schneeberger K, Ossowski S, Günther T, Bender S, Fitz J, et al. Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nat Genet. 2011;43:956-63.
70. Gan X, Stegle O, Behr J, Steffen JG, Drewe P, Hildebrand KL, et al. Multiple reference genomes and transcriptomes for Arabidopsis thaliana. Nature. 2011;477:419-23.
71. Long Q, Rabanal FA, Meng D, Huber CD, Farlow A, Platzer A, et al. Massive genomic variation and strong selection in Arabidopsis thaliana lines from Sweden. Nat Genet. 2013;45:884-90.
72. Hagmann J, Becker C, Muller J, Stegle O, Meyer RC, Wang G, et al. Century-scale methylome stability in a recently diverged Arabidopsis thaliana lineage. PLoS Genet. 2015;11:e1004920.
73. Dubin MJ, Zhang P, Meng D, Remigereau M-S, Osborne EJ, Paolo Casale F, et al. DNA methylation in Arabidopsis has a genetic basis and shows evidence of local adaptation. Elife. 2015;4:e05255.
74. 1001 Genomes Consortium. 1,135 genomes reveal the global pattern of polymorphism in Arabidopsis thaliana. Cell. 2016;166:481-91.
75. Kawakatsu T, Huang SC, Jupe F, Sasaki E, Schmitz RJ, Urich MA, et al. Epigenomic diversity in a global collection of Arabidopsis thaliana accessions. Cell. 2016;166:492-505.
76. Becker C, Hagmann J, Müller J, Koenig D, Stegle O, Borgwardt K, et al. Spontaneous epigenetic variation in the Arabidopsis thaliana methylome. Nature. 2011;480:245-9.
77. Schmitz RJ, Schultz MD, Lewsey MG, Malley RCO, Urich MA, Libiger O, et al. Transgenerational epigenetic instability is a source of novel methylation variants. Science. 2011;334:369-73.
78. Van der Graaf A, Wardenaar R, Neumann DA, Taudt A, Shaw RG, Jansen RC, et al. Rate, spectrum, and evolutionary dynamics of spontaneous epimutations. Proc Natl Acad Sci U S A. 2015;112:6676-81.
79. Schmitz RJ, He Y, Valdés-lópez O, Res G, Gent JI, Ellis NA, et al. Epigenome-wide inheritance of cytosine methylation variants in a recombinant inbred population. Genome Res. 2013;23:1663-74.
80. Virdi KS, Laurie JD, Xu Y-Z, Yu J, Shao M-R, Sanchez R, et al. Arabidopsis MSH1 mutation alters the epigenome and produces heritable changes in plant growth. Nat Commun. 2015;6:6386.
81. West PT, Li Q, Ji L, Eichten SR, Song J, Vaughn MW, et al. Genomic distribution of H3K9me2 and DNA methylation in a maize genome. PLoS One. 2014;9:1-10.
82. Li Q, Eichten SR, Hermanson PJ, Zaunbrecher VM, Song J, Wendt J, et al. Genetic perturbation of the maize methylome. Plant Cell. 2014;26:4602-16.
83. Li X, Zhu C, Yeh CT, Wu W, Takacs EM, Petsch KA, et al. Genic and nongenic contributions to natural variation of quantitative traits in maize. Genome Res. 2012;22:2436-44.
84. Bennetzen JL, Wang H. The contributions of transposable elements to the structure, function, and evolution of plant genomes. Annu Rev Plant Biol. 2014;65:505-30.
85. Wendel JF, Jackson SA, Meyers BC, Wing RA. Evolution of plant genome architecture. Genome Biol. 2016;17:37.
86. Bennetzen JL, Ma J, Devos KM. Mechanisms of recent genome size variation in flowering plants. Ann Bot. 2005;95:127-32.
87. Woo HR, Richards EJ. Natural variation in DNA methylation in ribosomal RNA genes of Arabidopsis thaliana. BMC Plant Biol. 2008;8:92.
88. Quadrana L, Bortolini Silveira A, Mayhew GF, LeBlanc C, Martienssen RA, Jeddeloh JA, et al. The Arabidopsis thaliana mobilome and its impact at the species level. Elife. 2016;5:e15716.
89. Stuart T, Eichten SR, Cahn J, Karpievitch Y, Borevitz JO, Lister R. Population scale mapping of novel transposable element diversity reveals links to gene regulation and epigenomic variation. bioRxiv. 2016; doi: http://dx.doi.org/10.1101/039511.
90. Mari-Ordóñez A, Marchais A, Etcheverry M, Martin A, Colot V, Voinnet O. Reconstructing de novo silencing of an active plant retrotransposon. Nat Genet. 2013;45:1029-39.
91. Hollister JD, Gaut BS. Epigenetic silencing of transposable elements: a trade-off between reduced transposition and deleterious effects on neighboring gene expression. Genome Res. 2009;19:1419-28.
92. Ahmed I, Sarazin A, Bowler C, Colot V, Quesneville H. Genome-wide evidence for local DNA methylation spreading from small RNA-targeted sequences in Arabidopsis. Nucleic Acids Res. 2011;39:6919-31.
93. Taudt A, Colomé-Tatché M, Johannes F. Genetic sources of population epigenomic variation. Nat Rev Genet. 2016;17:319-32.
94. Eichten SR, Briskine R, Song J, Li Q, Swanson-Wagner R, Hermanson PJ, et al. Epigenetic and genetic influences on DNA methylation variation in maize populations. Plant Cell. 2013;25:2783-97.
95. Stroud H, Do T, Du J, Zhong X, Feng S, Johnson L, et al. Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis. Nat Struct Mol Biol. 2014;21:64-72.
96. Hu L, Li N, Xu C, Zhong S, Lin X, Yang J, et al. Mutation of a major CG methylase in rice causes genome-wide hypomethylation, dysregulated genome expression, and seedling lethality. Proc Natl Acad Sci U S A. 2014;111:10642-7.
97. Bewick AJ, Ji L, Niederhuth CE, Willing E-M, 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;113:9111-6.
98. Lindroth AM, Cao X, Jackson JP, Zilberman D, McCallum CM, Henikoff S, et al. Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science. 2001;292:2077-80.
99. Shen X, De Jonge J, Forsberg SKG, Pettersson ME, Sheng Z, Hennig L, et al. Natural CMT2 variation is associated with genome-wide methylation changes and temperature seasonality. PLoS Genet. 2014;10:e1004842.
100. Jullien PE, Susaki D, Yelagandula R, Higashiyama T, Berger F. DNA methylation dynamics during sexual reproduction in Arabidopsis thaliana. Curr Biol. 2012;22:1825-30.
101. Papa CM, Springer NM, Muszynski MG, Meeley R, Kaeppler SM. Maize chromomethylase Zea methyltransferase2 is required for CpNpG methylation. Plant Cell. 2001;13:1919-28.
102. Matzke MA, Kanno T, Matzke AJM. RNA-directed DNA methylation: the evolution of a complex epigenetic pathway in flowering plants. Annu Rev Plant Biol. 2014;66:1-25.
103. Bewick AJ, Niederhuth CE, Rohr NA, Griffin PT, Leebens-Mack J, Schmitz RJ. The evolution of CHROMOMETHYLASES and gene body DNA methylation in plants. bioRxiv. 2016; doi: http://dx.doi.org/10.1101/054924.
104. Willing E-M, Rawat V, Mandáková T, Maumus F, James GV, Nordström KJV, et al. Genome expansion of Arabis alpina linked with retrotransposition and reduced symmetric DNA methylation. Nat Plants. 2015;1:14023.
105. Takuno S, Gaut BS. Body-methylated genes in Arabidopsis thaliana are functionally important and evolve slowly. Mol Biol Evol. 2012;29:219-27.
106. 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;110:1797-802.
107. Genereux DP, Miner BE, Bergstrom CT, Laird CD. A population-epigenetic model to infer site-specific methylation rates from double-stranded DNA methylation patterns. Proc Natl Acad Sci U S A. 2005;102:5802-7.
108. Meng D, Dubin M, Zhang P, Osborne EJ, Stegle O, Clark RM, et al. Limited contribution of DNA methylation variation to expression regulation in Arabidopsis thaliana. PLoS Genet. 2016;12:e1006141.
109. Cubas P, Vincent C, Coen E. An epigenetic mutation responsible for natural variation in floral symmetry. Nature. 1999;401:157-61.
110. Manning K, Tör M, Poole M, Hong Y, Thompson AJ, King GJ, et al. A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat Genet. 2006;38:948-52.
111. Eichten SR, Swanson-Wagner RA, Schnable JC, Waters AJ, Hermanson PJ, Liu S, et al. Heritable epigenetic variation among maize inbreds. PLoS Genet. 2011;7:e1002372.
112. Jiang C, Mithani A, Belfield EJ, Mott R, Hurst LD, Harberd NP. Environmentally responsive genome-wide accumulation of de novo Arabidopsis thaliana mutations and epimutations. Genome Res. 2014;24:1821-9.
113. Verhoeven KJF, Jansen JJ, van Dijk PJ, Biere A. Stress-induced DNA methylation changes and their heritability in asexual dandelions. New Phytol. 2010;185:1108-18.
114. Shaw RG, Byers DL, Darmo E. Spontaneous mutational effects on reproductive traits of Arabidopsis thaliana. Genetics. 2000;155:369-78.
115. Kawashima T, Berger F. Epigenetic reprogramming in plant sexual reproduction. Nat Rev Genet. 2014;15:613-24.
116. Ossowski S, Schneeberger K, Lucas-Lledó JI, Warthmann N, Clark RM, Shaw RG, et al. The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science. 2010;327:92-4.
117. Becker C, Weigel D. Epigenetic variation: origin and transgenerational inheritance. Curr Opin Plant Biol. 2012;15:562-7.
118. Estoup A, Jarne P, Cornuet JM. Homoplasy and mutation model at microsatellite loci and their consequences for population genetics analysis. Mol Ecol. 2002;11:1591-604.
119. Novikova PY, Hohmann N, Nizhynska V, Tsuchimatsu T, Ali J, Muir G, et al. Sequencing of the genus Arabidopsis identifies a complex history of nonbifurcating speciation and abundant trans-specific polymorphism. Nat Genet. 2016;48:1077-82.
120. Nordborg M, Hu TT, Ishino Y, Jhaveri J, Toomajian C, Zheng H, et al. The pattern of polymorphism in Arabidopsis thaliana. PLoS Biol. 2005;3:1289-99.
121. Wright S. Evolution in mendelian populations. Genetics. 1931;16:97-159.
122. Song YS, Steinrücken M. A simple method for finding explicit analytic transition densities of diffusion processes with general diploid selection. Genetics. 2012;190:1117-29.
123. Charlesworth B, Jain K. Purifying selection, drift, and reversible mutation with arbitrarily high mutation rates. Genetics. 2014;198:1587-602.
124. Wang J, Fan C. A neutrality test for detecting selection on DNA methylation using single methylation polymorphism frequency spectrum. Genome Biol Evol. 2014;7:154-71.
125. Kimura M. The number of heterozygous nucleotide sites maintained in a finite population due to steady flux of mutations. Genetics. 1969;61:893-903.
126. Wakeley J, Aliacar N. Gene genealogies in a metapopulation. Genetics. 2001;159:893-905.
127. Abramowitz M, Stegun IA. Handbook of mathematical functions. New York: Dover; 1965.
128. Živković D, Steinrücken M, Song YS, Stephan W. Transition densities and sample frequency spectra of diffusion processes with selection and variable population size. Genetics. 2015;200:601-17.