High-throughput sequencing of cytosine methylation in plant DNA

Plant Methods

Volumn 9, Issue 1, 2013, Pages

  Hardcastle, Thomas J ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84878643203     PISSN: None     EISSN: 17464811     Source Type: Journal    
DOI: 10.1186/1746-4811-9-16     Document Type: Review

References (82)

1. Cokus SJ, Feng S, Zhang X, Chen Z, Merriman B, Haudenschild CD, Pradhan S, Nelson SF, Pellegrini M, Jacobsen SE. Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 2008, 452(7184):215-219.
2. Lister R, O'Malley RC, Tonti-Filippini J, Gregory BD, Berry CC, Millar AH, Ecker JR. Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 2008, 133(3):523-536.
3. Jones L, Ratcliff F, Baulcombe DC. RNA-directed transcriptional gene silencing in plants can be inherited independently of the RNA trigger and requires Met1 for maintenance. Curr Biol 2001, 11(10):747-757.
4. Lindroth AM, Cao X, Jackson JP, Zilberman D, McCallum CM, Henikoff S, Jacobsen SE. Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science 2001, 292(5524):2077-2080.
5. Cao X, Aufsatz W, Zilberman D, Mette MF, Huang MS, Matzke M, Jacobsen SE. Role of the DRM and CMT3 methyltransferases in RNA-directed DNA methylation. Curr Biol 2003, 13(24):2212-2217.
6. Pontes O, Li CF, Costa Nunes P, Haag J, Ream T, Vitins A, Jacobsen SE, Pikaard CS. The Arabidopsis chromatin-modifying nuclear siRNA pathway involves a nucleolar RNA processing center. Cell 2006, 126:79-92.
7. Gong Z, Morales-Ruiz T, Ariza RR, Roldán-Arjona T, David L, Zhu JK. ROS1, a repressor of transcriptional gene silencing in Arabidopsis, encodes a DNA glycosylase/lyase. Cell 2002, 111(6):803-814.
8. Choi Y, Gehring M, Johnson L, Hannon M, Harada JJ, Goldberg RB, Jacobsen SE, Fischer RL. DEMETER, a DNA Glycosylase domain protein, Is required for Endosperm gene imprinting and seed viability in Arabidopsis. Cell 2002, 110:33-42.
9. Ortega-Galisteo AP, Morales-Ruiz T, Ariza RR, Roldán-Arjona T. Arabidopsis DEMETER-LIKE proteins DML2 and DML3 are required for appropriate distribution of DNA methylation marks. Plant Mol Biol 2008, 67(6):671-681.
10. Morales-Ruiz T, Ortega-Galisteo AP, Ponferrada-Marín MI, Martínez-Macías MI, Ariza RR, Roldán-Arjona T. DEMETER and REPRESSOR OF SILENCING 1 encode 5-methylcytosine DNA glycosylases. Proc Natl Acad Sci U S A 2006, 103(18):6853-6858.
11. Zheng X, Pontes O, Zhu J, Miki D, Zhang F, Li WX, Iida K, Kapoor A, Pikaard CS, Zhu JK. ROS3 is an RNA-binding protein required for DNA demethylation in Arabidopsis. Nature 2008, 455(7217):1259-1262.
12. Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan SWL, Chen H, Henderson IR, Shinn P, Pellegrini M, Jacobsen SE, Ecker JR. Genome-wide high-resolution mapping and functional analysis of DNA methylation in arabidopsis. Cell 2006, 126(6):1189-1201.
13. Berdasco M, Alcázar R, García-Ortiz MV, Ballestar E, Fernández AF, Roldán-Arjona T, Tiburcio AF, Altabella T, Buisine N, Quesneville H, Baudry A, Lepiniec L, Alaminos M, Rodríguez R, Lloyd A, Colot V, Bender J, Canal MJ, Esteller M, Fraga MF. Promoter DNA hypermethylation and gene repression in undifferentiated Arabidopsis cells. PloS One 2008, 3(10):e3306.
14. Tsukahara S, Kobayashi A, Kawabe A, Mathieu O, Miura A, Kakutani T. Bursts of retrotransposition reproduced in Arabidopsis. Nature 2009, 461(September):3-7.
15. Zemach A, McDaniel IE, Silva P, Zilberman D. Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science 2010, 328(5980):916-919.
16. González RM, Ricardi MM, Iusem ND. Atypical epigenetic mark in an atypical location: cytosine methylation at asymmetric (CNN) sites within the body of a non-repetitive tomato gene. BMC Plant Biol 2011, 11:94.
17. Kou HP, Li Y, Song XX, Ou XF, Xing SC, Ma J, Von Wettstein D, Liu B. Heritable alteration in DNA methylation induced by nitrogen-deficiency stress accompanies enhanced tolerance by progenies to the stress in rice (Oryza sativa L.). J Plant Physiol 2011, 168(14):1685-1693.
18. Karan R, DeLeon T, Biradar H, Subudhi PK. Salt stress induced variation in DNA methylation pattern and its influence on gene expression in contrasting rice genotypes. PloS One 2012, 7(6):e40203.
19. Dowen RH, Pelizzola M, Schmitz RJ, Lister R, Dowen JM, Nery JR, Dixon JE, Ecker JR. Widespread dynamic DNA methylation in response to biotic stress. Proc Natl Acad Sci U S A 2012, 109(32):E2183-E2191.
20. Kathiria P, Sidler C, Golubov A, Kalischuk M, Kawchuk LM, Kovalchuk I. Tobacco mosaic virus infection results in an increase in recombination frequency and resistance to viral, bacterial, and fungal pathogens in the progeny of infected tobacco plants. Plant Physiol 2010, 153(4):1859-1870.
21. Shen H, He H, Li J, Chen W, Wang X, Guo L, Peng Z, He G, Zhong S, Qi Y, Terzaghi W, Deng XW. Genome-wide analysis of DNA methylation and gene expression changes in two Arabidopsis ecotypes and their reciprocal hybrids. Plant Cell 2012, 24(3):875-892.
22. Huh JH, Bauer MJ, Hsieh TF, Fischer RL. Cellular programming of plant gene imprinting. Cell 2008, 132(5):735-744.
23. Hamilton A, Voinnet O, Chappell L, Baulcombe D. Two classes of short interfering RNA in RNA silencing. EMBO J 2002, 21(17):4671-4679.
24. Chan SWL, Zilberman D, Xie Z, Johansen LK, Carrington JC, Jacobsen SE. RNA silencing genes control de novo DNA methylation. Science 1336, 303(5662).
25. Tran RK, Henikoff JG, Zilberman D, Ditt RF, Jacobsen SE, Henikoff S. DNA methylation profiling identifies CG methylation clusters in Arabidopsis genes. Curr Biol 2005, 15(2):154-159.
26. 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, 39:61-69.
27. Clark SJ, Statham A, Stirzaker C, Molloy PL, Frommer M. DNA methylation: bisulphite modification and analysis. Nature Protoc 2006, 1(5):2353-2364.
28. Frommer M, McDonald LE, Millar DS, Collis CM, Watt F, Grigg GW, Molloy PL, Paul CL. A genomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands. Proc Natl Acad Sci U S A 1992, 89(5):1827-1231.
29. Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, Agarwal S, Iyer LM, Liu DR, Aravind L, Rao A. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 2009, 324(5929):930-935.
30. Kriaucionis S, Heintz N. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 2009, 324(5929):929-930.
31. Huang Y, Pastor WA, Shen Y, Tahiliani M, Liu DR, Rao A. The behaviour of 5-hydroxymethylcytosine in bisulfite sequencing. PloS One 2010, 5:e8888.
32. Jeddeloh JA, Greally JM, Rando OJ. Reduced-representation methylation mapping. Genome Biol 2008, 9(8):231.
33. Meissner A, Gnirke A, Bell GW, Ramsahoye B, Lander ES, Jaenisch R. Reduced representation bisulfite sequencing for comparative high-resolution DNA methylation analysis. Nucleic Acids Res 2005, 33(18):5868-5877.
34. Gu H, Smith ZD, Bock C, Boyle P, Gnirke A, Meissner A. Preparation of reduced representation bisulfite sequencing libraries for genome-scale DNA methylation profiling. Nature Protoc 2011, 6(4):468-481.
35. Teer JK, Bonnycastle LL, Chines PS, Hansen NF, Aoyama N, Swift AJ, Abaan HO, Albert TJ, Margulies EH, Green ED, Collins FS, Mullikin JC, Biesecker LG. Systematic comparison of three genomic enrichment methods for massively parallel DNA sequencing. Genome Res 2010, 20(10):1420-1431.
36. Lee EJ, Pei L, Srivastava G, Joshi T, Kushwaha G, Choi JH, Robertson KD, Wang X, Colbourne JK, Zhang L, Schroth GP, Xu D, Zhang K, Shi H. Targeted bisulfite sequencing by solution hybrid selection and massively parallel sequencing. Nucleic Acids Res 2011, 39(19):e127.
37. Wang J, Jiang H, Ji G, Gao F, Wu M, Sun J, Luo H, Wu J, Wu R, Zhang X. High resolution profiling of human exon methylation by liquid hybridization capture-based bisulfite sequencing. BMC Genomics 2011, 12:597.
38. Ivanov M, Kals M, Kacevska M, Metspalu A, Ingelman-Sundberg M, Milani L. In-solution hybrid capture of bisulfite-converted DNA for targeted bisulfite sequencing of 174 ADME genes. Nucleic Acids Res 2013, 41(6):e72.
39. Down TA, Rakyan VK, Turner DJ, Flicek P, Li H, Kulesha E, Gräf S, Johnson N, Herrero J, Tomazou EM, Thorne NP, Bäckdahl L, Herberth M, Howe KL, Jackson DK, Miretti MM, Marioni JC, Birney E, Hubbard TJP, Durbin R, Beck S, . Tavaré S A Bayesian deconvolution strategy for immunoprecipitation-based DNA methylome analysis. Nat Biotechnol 2008, 26(7):779-785. Tavaré S.
40. Taiwo O, Wilson GA, Morris T, Seisenberger S, Reik W, Pearce D, Beck S, Butcher LM. Methylome analysis using MeDIP-seq with low DNA concentrations. Nature Protoc 2012, 7(4):617-636.
41. Serre D, Lee BH, Ting AH. MBD-isolated Genome Sequencing provides a high-throughput and comprehensive survey of DNA methylation in the human genome. Nucleic Acids Res 2010, 38(2):391-399.
42. Brinkman AB, Simmer F, Ma K, Kaan A, Zhu J, Stunnenberg HG. Whole-genome DNA methylation profiling using MethylCap-seq. Methods 2010, 52(3):232-236.
43. Reinders J, Delucinge Vivier C, Theiler G, Chollet D, Descombes P, Paszkowski J. Genome-wide, high-resolution DNA methylation profiling using bisulfite-mediated cytosine conversion. Genome Res 2008, 18(3):469-476.
44. Stroud H, Greenberg M, Feng S, Bernatavichute Y, Jacobsen S. Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell 2013, 152:352-364.
45. Havecker ER, Wallbridge LM, Fedito P, Hardcastle TJ, Baulcombe DC. Metastable Differentially methylated regions within Arabidopsis inbred populations are associated with modified expression of non-coding transcripts. PloS One 2012, 7(9):e45242.
46. Schmitz RJ, Schultz MD, Lewsey MG, O'Malley RC, Urich MA, Libiger O, Schork NJ, Ecker JR. Transgenerational epigenetic instability is a source of novel methylation variants. Science 2011, 334(6054):369-373.
47. Becker C, Hagmann J, Müller J, Koenig D, Stegle O, Borgwardt K, Weigel D. Spontaneous epigenetic variation in the Arabidopsis thaliana methylome. Nature 2011, 480(7376):245-249.
48. Eichten SR, Swanson-Wagner RA, Schnable JC, Waters AJ, Hermanson PJ, Liu S, Yeh CT, Jia Y, Gendler K, Freeling M, Schnable PS, Vaughn MW, Springer NM. Heritable epigenetic variation among maize inbreds. PLoS Genetics 2011, 7(11):e1002372.
49. Feng S, Cokus SJ, Zhang X, Chen PY, Bostick M, Goll MG, Hetzel J, Jain J, Strauss SH, Halpern ME, Ukomadu C, Sadler KC, Pradhan S, Pellegrini M, Jacobsen SE. Conservation and divergence of methylation patterning in plants and animals. Proc Natl Acad Sci U S A 2010, 107(19):8689-8694.
50. Nishiyama R, Wada Y, Mibu M, Yamaguchi Y, Shimogawara K, Sano H. Role of a nonselective de novo DNA methyltransferase in maternal inheritance of chloroplast genes in the green alga, Chlamydomonas reinhardtii. Genetics 2004, 168(2):809-816.
51. Krueger F, Kreck B, Franke A, Andrews SR. DNA methylome analysis using short bisulfite sequencing data. Nat Methods 2012, 9(2):145-151.
52. Chatterjee A, Stockwell PA, Rodger EJ, Morison IM. Comparison of alignment software for genome-wide bisulphite sequence data. Nucleic Acids Res 2012, 40(10):e79.
53. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009, 10(3):R25.
54. Chen PY, Cokus SJ, Pellegrini M. BS Seeker: precise mapping for bisulfite sequencing. BMC Bioinformatics 2010, 11:203.
55. Krueger F, Andrews SR. Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics 2011, 27(11):1571-1572.
56. Pedersen B, Hsieh TF, Ibarra C, Fischer RL. MethylCoder: software pipeline for bisulfite-treated sequences. Bioinformatics 2011, 27(17):2435-2436.
57. Hansen KD, Langmead B, Irizarry RA. BSmooth: from whole genome bisulfite sequencing reads to differentially methylated regions. Genome Biol 2012, 13(10):R83.
58. Xi Y, Li W. BSMAP: whole genome bisulfite sequence MAPping program. BMC Bioinformatics 2009, 10:232.
59. M Burrows DJW. A block-sorting lossless data compression algorithm. Technical Report 1994,
60. Harris EY, Ponts N, Le Roch KG, Lonardi S. BRAT-BW: Efficient and accurate mapping of bisulfite-treated reads. Bioinformatics 2012, 28(13):1795-1796.
61. Dinh HQ, Dubin M, Sedlazeck FJ, Lettner N, Mittelsten Scheid O, von Haeseler A. Advanced methylome analysis after bisulfite deep sequencing: an example in Arabidopsis. PloS One 2012, 7(7):e41528.
62. Smith AD, Chung WY, Hodges E, Kendall J, Hannon G, Hicks J, Xuan Z, Zhang MQ. Updates to the RMAP short-read mapping software. Bioinformatics 2009, 25(21):2841-2842.
63. Frith MC, Mori R, Asai K. A mostly traditional approach improves alignment of bisulfite-converted DNA. Nucleic Acids Res 2012, 40(13):e100.
64. Smith AM, Heisler LE, Mellor J, Kaper F, Thompson MJ, Chee M, Roth FP, Giaever G, Nislow C. Quantitative phenotyping via deep barcode sequencing. Genome Res 2009, 19(10):1836-1842.
65. Valouev A, Ichikawa J, Tonthat T, Stuart J, Ranade S, Peckham H, Zeng K, Malek JA, Costa G, McKernan K, Sidow A, Fire A, Johnson SM. A high-resolution, nucleosome position map of C. elegans reveals a lack of universal sequence-dictated positioning. Genome Res 2008, 18(7):1051-1063.
66. Bormann Chung CA, Boyd VL, McKernan KJ, Fu Y, Monighetti C, Peckham HE, Barker M. Whole methylome analysis by ultra-deep sequencing using two-base encoding. PloS One 2010, 5(2):e9320.
67. Ondov BD, Cochran C, Landers M, Meredith GD, Dudas M, Bergman NH. An alignment algorithm for bisulfite sequencing using the Applied Biosystems SOLiD System. Bioinformatics 2010, 26(15):1901-1902.
68. Kreck B, Marnellos G, Richter J, Krueger F, Siebert R, Franke A. B-SOLANA: an approach for the analysis of two-base encoding bisulfite sequencing data. Bioinformatics 2012, 28(3):428-429.
69. Campagna D, Telatin A, Forcato C, Vitulo N, Valle G. PASS-bis: a bisulfite aligner suitable for whole methylome analysis of Illumina and solid reads. Bioinformatics 2013, 29(2):268-270.
70. Minoche AE, Dohm JC, Himmelbauer H. Evaluation of genomic high-throughput sequencing data generated on Illumina HiSeq and genome analyzer systems. Genome Biol 2011, 12(11):R112.
71. Wang XV, Blades N, Ding J, Sultana R, Parmigiani G. Estimation of sequencing error rates in short reads. BMC Bioinformatics 2012, 13:185.
72. Kovarik A, Matyásek R, . Fojtová M Cytosine methylation of plastid genome in higher plants. Fact or artefact?. Plant Sci 2001, 160(4):585-593. Fojtová M.
73. Bock C. Analysing and interpreting DNA methylation data. Nat Rev Genet 2012, 13(10):705-719.
74. Robinson MD, Smyth GK. Moderated statistical tests for assessing differences in tag abundance. Bioinformatics 2007, 23(21):2881-2887.
75. Hardcastle TJ, Kelly KA. baySeq: empirical Bayesian methods for identifying differential expression in sequence count data. BMC Bioinformatics 2010, 11:422.
76. Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol 2010, 11(10):R106.
77. McCarthy DJ, Chen Y, Smyth GK. Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucleic Acids Res 2012, 40(10):4288-4297.
78. Hardcastle TJ, Kelly KA. Empirical Bayesian analysis of paired high-throughput sequencing data with a beta-binomial distribution. BMC Bioinformatics 2013, in press.
79. Wetterstrand K. DNA sequencing costs: data from the NHGRI Genome sequencing program (GSP). 2013, [http://www.genome.gov/sequencingcosts/].
80. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 2008, 5(7):621-628.
81. Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 2011, 12:323.
82. Kim H, Bi Y, Pal S, Gupta R, Davuluri RV. IsoformEx: isoform level gene expression estimation using weighted non-negative least squares from mRNA-Seq data. BMC Bioinformatics 2011, 12:305.