Methylome of DNase I sensitive chromatin in Populus trichocarpa shoot apical meristematic cells: A simplified approach revealing characteristics of gene-body DNA methylation in open chromatin state

New Phytologist

Volumn 197, Issue 2, 2013, Pages 416-430

  Lafon Placette, Clément ^a,b   Faivre Rampant, Patricia ^c   Delaunay, Alain ^a,b   Street, Nathaniel ^d   Brignolas, Franck ^a,b   Maury, Stéphane ^a,b  

^a UNIVERSITÉ D'ORLÉANS   (France)

^b CEMAGREF   (France)

^c UNIVERSITÉ D EVRY VAL D ESSONNE   (France)

^d UMEÅ UNIVERSITY   (Sweden)

Author keywords

DNA methylation; Genes; Methylome; Open chromatin; Populus trichocarpa (black cottonwood); Shoot apical meristem

Indexed keywords

CYTOSINE; DEOXYRIBONUCLEASE I; MESSENGER RNA;

ADAPTATION; DATA PROCESSING; DNA; GENE; GENE EXPRESSION; ISOLATION EFFECT; MAPPING; METHYLATION; PERENNIAL PLANT; SHOOT;

ARTICLE; BIOLOGICAL MODEL; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOME MAP; CROSS BREEDING; CYTOLOGY; DNA METHYLATION; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENETIC VARIABILITY; GENETICS; HYBRIDIZATION; MERISTEM; METABOLISM; NUCLEOTIDE SEQUENCE; PLANT GENE; POPULUS; REPRODUCIBILITY;

BASE SEQUENCE; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOME MAPPING; CROSSES, GENETIC; CYTOSINE; DEOXYRIBONUCLEASE I; DNA METHYLATION; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENETIC VARIATION; HYBRIDIZATION, GENETIC; MERISTEM; MODELS, GENETIC; POPULUS; REPRODUCIBILITY OF RESULTS; RNA, MESSENGER; SEQUENCE ANALYSIS, DNA;

POPULUS TRICHOCARPA;

EID: 84871294329     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12026     Document Type: Article

References (54)

1. Abrouk M, Murat F, Pont C, Messing J, Jackson S, Faraut T, Tannier E, Plomion C, Cooke R, Feuillet C. 2010. Palaeogenomics of plants: synteny-based modelling of extinct ancestors. Trends in Plant Science 15: 479-487.
2. Beck S, Rakyan VK. 2008. The methylome: approaches for global DNA methylation profiling. Trends in Genetics 24: 231-237.
3. Bennett S. 2004. Solexa Ltd. Pharmacogenomics 5: 433-438.
4. Causevic A, Delaunay A, Ounnar S, Righezza M, Delmotte F, Brignolas F, Hagège D, Maury S. 2005. DNA methylating and demethylating treatments modify phenotype and cell wall differentiation state in sugarbeet cell lines. Plant Physiology and Biochemistry: PPB/Société Française De Physiologie Végétale 43: 681-691.
5. Causevic A, Gentil M-V, Delaunay A, El-Soud WA, Garcia Z, Pannetier C, Brignolas F, Hagège D, Maury S. 2006. Relationship between DNA methylation and histone acetylation levels, cell redox and cell differentiation states in sugarbeet lines. Planta 224: 812-827.
6. Chodavarapu RK, Feng S, Bernatavichute YV, Chen P-Y, Stroud H, Yu Y, Hetzel JA, Kuo F, Kim J, Cokus SJ et al. 2010. Relationship between nucleosome positioning and DNA methylation. Nature 466: 388-392.
7. Cokus SJ, Feng S, Zhang X, Chen Z, Merriman B, Haudenschild CD, Pradhan S, Nelson SF, Pellegrini M, Jacobsen SE. 2008. Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452: 215-219.
8. Costas C, De La Paz Sanchez M, Stroud H, Yu Y, Oliveros JC, Feng S, Benguria A, López-Vidriero I, Zhang X, Solano R et al. 2011. Genome-wide mapping of Arabidopsis thaliana origins of DNA replication and their associated epigenetic marks. Nature Structural & Molecular Biology 18: 395-400.
9. Crawford GE, Davis S, Scacheri PC, Renaud G, Halawi MJ, Erdos MR, Green R, Meltzer PS, Wolfsberg TG, Collins FS. 2006. DNase-chip: a high-resolution method to identify DNase I hypersensitive sites using tiled microarrays. Nature Methods 3: 503-509.
10. Crawford GE, Holt IE, Mullikin JC, Tai D, Blakesley R, Bouffard G, Young A, Masiello C, Green ED, Wolfsberg TG et al. 2004. Identifying gene regulatory elements by genome-wide recovery of DNase hypersensitive sites. Proceedings of the National Academy of Sciences, USA 101: 992-997.
11. Dembinsky D, Woll K, Saleem M, Liu Y, Fu Y, Borsuk LA, Lamkemeyer T, Fladerer C, Madlung J, Barbazuk B et al. 2007. Transcriptomic and proteomic analyses of pericycle cells of the maize primary root. Plant physiology 145: 575-588.
12. Dimitrovna AD, Ananiev ED, Gecheff KI. 2009. DNase I hypersensitive sites within the intergenic spacer of ribosomal RNA genes in reconstructed barley karyotypes. Biotechnology & Biotechnological Equipment 23: 1039-1043.
13. Faivre-Rampant P, Jeandroz S, Lefevre F, Lemoine M, Villar M, Berville A. 1992. Ribosomal DNA studies in poplars: Populus deltoides, P. nigra, P. trichocarpa, P. maximowiczii, and P. alba. Genome 35: 733-740.
14. Feng S, Cokus SJ, Zhang X, Chen P-Y, Bostick M, Goll MG, Hetzel J, Jain J, Strauss SH, Halpern ME et al. 2010a. Conservation and divergence of methylation patterning in plants and animals. Proceedings of the National Academy of Sciences, USA 107: 8689-8694.
15. Feng S, Jacobsen SE, Reik W. 2010b. Epigenetic reprogramming in plant and animal development. Science 330: 622-627.
16. Galbraith DW, Harkins KR, Maddox JM, Ayres NM, Sharma DP, Firoozabady E. 1983. Rapid flow cytometric analysis of the cell cycle in intact plant tissues. Science (New York, N.Y.) 220: 1049-1051.
17. Goll MG, Bestor TH. 2005. Eukaryotic cytosine methyltransferases. Annual Review of Biochemistry 74: 481-514.
18. Gourcilleau D, Bogeat-Triboulot M-B, Le Thiec D, Lafon-Placette C, Delaunay A, El-Soud WA, Brignolas F, Maury S. 2010. DNA methylation and histone acetylation: genotypic variations in hybrid poplars, impact of water deficit and relationships with productivity. Annals of Forest Science 67: 208.
19. Hamanishi ET, Campbell MM. 2011. Genome-wide responses to drought in forest trees. Forestry 84: 273-283.
20. Hernandez D, François P, Farinelli L, Osterås M, Schrenzel J. 2008. De novo bacterial genome sequencing: millions of very short reads assembled on a desktop computer. Genome research 18: 802-809.
21. Islam-Faridi MN, Nelson CD, DiFazio SP, Gunter LE, Tuskan GA. 2009. Cytogenetic analysis of Populus trichocarpa - ribosomal DNA, telomere repeat sequence, and marker-selected BACs. Cytogenetic and Genome Research 125: 74-80.
22. Jansson S, Douglas CJ. 2007. Populus: a model system for plant biology. Annual Review of Plant Biology 58: 435-458.
23. Jin C, Zang C, Wei G, Cui K, Peng W, Zhao K, Felsenfeld G. 2009. H3.3/H2A.Z double variant-containing nucleosomes mark 'nucleosome-free regions' of active promoters and other regulatory regions. Nature Genetics 41: 941-945.
24. Klevebring D, Street NR, Fahlgren N, Kasschau KD, Carrington JC, Lundeberg J, Jansson S. 2009. Genome-wide profiling of Populus small RNAs. BMC Genomics 10: 620.
25. Lechner T, Lusser A, Pipal A, Brosch G, Loidl A, Goralik-Schramel M, Sendra R, Wegener S, Walton JD, Loidl P. 2000. RPD3-type histone deacetylases in maize embryos. Biochemistry 39: 1683-1692.
26. Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, Tonti-Filippini J, Nery JR, Lee L, Ye Z, Ngo Q-M et al. 2009. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462: 315-322.
27. Loureiro J, Rodriguez E, Dolezel J, Santos C. 2007. Two new nuclear isolation buffers for plant DNA flow cytometry: a test with 37 species. Annals of Botany 100: 875-888.
28. Mathieu O, Yukawa Y, Sugiura M, Picard G, Tourmente S. 2002. 5S rRNA genes expression is not inhibited by DNA methylation in Arabidopsis. Plant Journal: For Cell and Molecular Biology 29: 313-323.
29. Miura A, Nakamura M, Inagaki S, Kobayashi A, Saze H, Kakutani T. 2009. An Arabidopsis jmjC domain protein protects transcribed genes from DNA methylation at CHG sites. The EMBO Journal 28: 1078-1086.
30. Morse AM, Peterson DG, Islam-Faridi MN, Smith KE, Magbanua Z, Garcia SA, Kubisiak TL, Amerson HV, Carlson JE, Nelson CD et al. 2009. Evolution of genome size and complexity in Pinus. PLoS ONE 4: e4332.
31. Pecinka A, Dinh HQ, Baubec T, Rosa M, Lettner N, Mittelsten Scheid O. 2010. Epigenetic regulation of repetitive elements is attenuated by prolonged heat stress in Arabidopsis. The Plant Cell 22: 3118-3129.
32. Penterman J, Zilberman D, Huh JH, Ballinger T, Henikoff S, Fischer RL. 2007. DNA demethylation in the Arabidopsis genome. Proceedings of the National Academy of Sciences, USA 104: 6752-6757.
33. Qian J, Lavker RM, Tseng H. 2006. Mapping ribosomal RNA transcription activity in the mouse eye. Developmental Dynamics: An Official Publication of the American Association of Anatomists 235: 1984-1993.
34. Raj S, Brautigam K, Hamanishi ET, Wilkins O, Thomas BR, Schroeder W, Mansfield SD, Plant AL, Campbell MM. 2011. Clone history shapes Populus drought responses. Proceedings of the National Academy of Sciences, USA 108: 12521-12526.
35. Roudier F, Ahmed I, Bérard C, Sarazin A, Mary-Huard T, Cortijo S, Bouyer D, Caillieux E, Duvernois-Berthet E, Al-Shikhley L et al. 2011. Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. The EMBO Journal 30: 1928-1938.
36. Sati S, Tanwar VS, Kumar KA, Patowary A, Jain V, Ghosh S, Ahmad S, Singh M, Reddy SU, Chandak GR et al. 2012. High resolution methylome map of rat indicates role of intragenic DNA methylation in identification of coding region. PLoS ONE 7: e31621.
37. Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves TA et al. 2009. The B73 Maize genome: complexity, diversity, and dynamics. Science 326: 1112-1115.
38. Sjödin A, Street NR, Sandberg G, Gustafsson P, Jansson S. 2009. The Populus genome integrative explorer (PopGenIE): a new resource for exploring the Populus genome. New Phytologist 182: 1013-1025.
39. Steinmuller K, Apel K. 1986. A simple and efficient procedure for isolating plant chromatin which is suitable for studies of DNase I-sensitive domains and hypersensitive sites. Plant Molecular Biology 7: 87-94.
40. Street N, Sjödin A, Bylesjö M, Gustafsson P, Trygg J, Jansson S. 2008. A cross-species transcriptomics approach to identify genes involved in leaf development. BMC Genomics 9: 589.
41. Suzuki MM, Bird A. 2008. DNA methylation landscapes: provocative insights from epigenomics. Nature Reviews Genetics 9: 465-476.
42. Teixeira FK, Colot V. 2010. Repeat elements and the Arabidopsis DNA methylation landscape. Heredity 105: 14-23.
43. Trap-Gentil M-V, Hébrard C, Lafon-Placette C, Delaunay A, Hagège D, Joseph C, Brignolas F, Lefebvre M, Barnes S, Maury S. 2011. Time course and amplitude of DNA methylation in the shoot apical meristem are critical points for bolting induction in sugar beet and bolting tolerance between genotypes. Journal of Experimental Botany 62: 2585-2597.
44. Tucker S, Vitins A, Pikaard CS. 2010. Nucleolar dominance and ribosomal RNA gene silencing. Current Opinion in Cell Biology 22: 351-356.
45. Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A et al. 2006. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313: 1596-1604.
46. Vining KJ, Pomraning KR, Wilhelm LJ, Priest HD, Pellegrini M, Mockler TC, Freitag M, Strauss S. 2012. Dynamic DNA cytosine methylation in the Populus trichocarpa genome: tissue-level variation and relationship to gene expression. BMC Genomics 13: 27.
47. Weng Y-I, Huang TH-M, Yan PS. 2009. Methylated DNA immunoprecipitation and microarray-based analysis: detection of DNA methylation in breast cancer cell lines. Methods in Molecular Biology (Clifton, N.J.) 590: 165-176.
48. Woo HR, Dittmer TA, Richards EJ. 2008. Three SRA-domain methylcytosine-binding proteins cooperate to maintain global CpG methylation and epigenetic silencing in Arabidopsis (T Kakutani, Ed.). PLoS Genetics 4: e1000156.
49. Zemach A, McDaniel IE, Silva P, Zilberman D. 2010. Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science 328: 916-919.
50. Zhang X, Shiu S, Cal A, Borevitz JO. 2008. Global analysis of genetic, epigenetic and transcriptional polymorphisms in Arabidopsis thaliana using whole genome tiling arrays (GP Copenhaver, Ed.). PLoS Genetics 4: e1000032.
51. Zhang W, Wu Y, Schnable JC, Zeng Z, Freeling M, Crawford GE, Jiang J. 2012a. High-resolution mapping of open chromatin in the rice genome. Genome research 22: 151-162.
52. Zhang W, Zhang T, Wu Y, Jiang J. 2012b. Genome-wide identification of regulatory DNA elements and protein-binding footprints using signatures of open chromatin in Arabidopsis. The Plant Cell 24: 2719-2731.
53. Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan SW-L, Chen H, Henderson IR, Shinn P, Pellegrini M, Jacobsen SE et al. 2006. Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126: 1189-1201.
54. Zilberman D, Gehring M, Tran RK, Ballinger T, Henikoff S. 2007. Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nature Genetics 39: 61-69.