Genic DNA methylation changes during in vitro organogenesis: Organ specificity and conservation between parental lines of epialleles

Physiologia Plantarum

Volumn 146, Issue 3, 2012, Pages 321-335

  Maury, Stéphane ^a   Trap Gentil, Marie Véronique ^a   Hébrard, Claire ^a,b   Weyens, Guy ^b   Delaunay, Alain ^a   Barnes, Steve ^b   Lefebvre, Marc ^b   Joseph, Claude ^a  

^a UNIVERSITÉ D'ORLÉANS   (France)

^b SESVanderHave NV/SA   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

PLANT DNA;

ALLELE; ANTIBODY SPECIFICITY; ARTICLE; BEET; CELL DIFFERENTIATION; CHEMISTRY; CPG ISLAND; CULTURE TECHNIQUE; DNA METHYLATION; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; PHENOTYPE; PHYSIOLOGY; PLANT; PLANT ROOT; REGENERATION; TRANSGENIC PLANT;

ALLELES; BETA VULGARIS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CPG ISLANDS; DNA METHYLATION; DNA, PLANT; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, PLANT; ORGAN SPECIFICITY; PHENOTYPE; PLANT ROOTS; PLANT SHOOTS; PLANTS, GENETICALLY MODIFIED; REGENERATION; SEQUENCE ANALYSIS, DNA;

ARABIDOPSIS; BETA VULGARIS; BETA VULGARIS SUBSP. VULGARIS;

EID: 84867208981     PISSN: 00319317     EISSN: 13993054     Source Type: Journal    
DOI: 10.1111/j.1399-3054.2012.01634.x     Document Type: Article

References (62)

1. Abe T, Matsuyama T, Sekido S, Yamaguchi I, Yoshida S, Kameya T (2002) Chlorophyll-deficient mutants of rice demonstrated the deletion of a DNA fragment by heavy-ion irradiation. J Radiat Res 43: 157-161
2. Ashikawa, I (2001) Gene-associated CpG islands in plants as revealed by analyses of genomic sequences. Plant J 26: 617-625
3. Avivi Y, Morad V, Ben-Meir H, Zhao J, Kashkush K, Tzfira T, Citovsky V, Grafi G (2004) Reorganization of specific chromosomal domains and of silent genes in plant cells acquiring pluripotentiality. Dev Dyn 230: 12-22
4. Becker C, Hagmann J, Müller J, Koenig D, Stegle O, Borgwardt K, Weigel D (2011) Spontaneous epigenetic variation in the Arabidopsis thaliana methylome. Nature 480: 245-251
5. Berdasco M, Alcazar R, Garcia-Ortiz MV, Ballestar E, Fernandez AF, Roldan-Arjona T, Tiburcio AF, Altabella T, Buisine N, Quesneville H, Baudry A, Lepiniec L, Alaminos M, Rodriguez R, Lloyd A, Colot V, Bender J, Canal MJ, Esteller M, Fraga MF (2008) Promoter DNA hypermethylation and gene repression in undifferentiated Arabidopsis cells. PLoS ONE 3:e3306. DOI: 10.1371/journal.pone.0003306
6. Brown DCW, Thorpe TA (1995) Crop improvement through tissue culture. World J Microbiol Biotechnol 11: 409-415
7. Callis J, Raash JA, Vietstra RD (1990) Ubiquitin extension proteins of Arabidopsis thaliana. J Biol Chem 265: 12486-12493
8. Capitani F, Biondi S, Falasca G, Ziosi V, Balestrazzi A, Carbonera D, Torrigiani P, Altamura MM (2005) Methyl jasmonate disrupts shoot formation in tobacco thin cell layers by over-inducing mitotic activity and cell expansion. Planta 220: 507-519
9. 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 Physiol Biochem 43: 681-691
10. 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. Planta 224: 812-827
11. Cerrie B, Gaspar T, Greppin H, Penel C (1994) Redox characteristic of normal and habituated cell lines of sugarbeet. Plant Cell Environ 17: 457-461
12. Che P, Lall S, Nettleton D, Howell SH (2006) Gene expression programs during shoot, root, and callus development in Arabidopsis tissue culture. Plant Physiol 141: 620-637
13. Chodavarapu RK, Feng S, Bernatavichute YV, Chen PY, Stroud H, Yu Y, Hetzel J, Kuo F, Kim J, Cokus SJ, Casero D, Bernal M, Huijser P, Clark AT, Krämer U, Merchant SS, Zhang X, Jacobsen SE, Pellegrini M (2010) Relationship between nucleosome positioning and DNA methylation. Nature 466: 388-392
14. Costa S, Shaw P (2007) 'Open minded' cells: how cells can change fate. Trends Cell Biol 17: 101-106
15. Costello J, Smiraglia D, Plass C (2002) Restriction landmark genome scanning. Methods 27: 144-149
16. Dodsworth S (2009) A diverse and intricate signalling network regulates stem cell fate in the shoot apical meristem. Dev Biol 336: 1-9
17. Feng S, Jacobsen SE, Reik W (2010) Epigenetic reprogramming in plant and animal development. Science 330: 622-627
18. Finnegan EJ, Kovac KA, Jaligot E, Sheldon CC, Peacock WJ, Dennis ES (2005) The downregulation of FLOWERING LOCUS C (FLC) expression in plants with low levels of DNA methylation and by vernalization occurs by distinct mechanisms. Plant J 44: 420-432
19. Fraga MF, Rodriguez R, Canal MJ (2002) Genomic DNA methylation-demethylation during aging and reinvigoration of Pinus radiata. Tree Physiol 22: 813-816
20. Gentil M-V, Maury S(2007) Characterization of epigenetic biomarkers using new molecular approaches. In: Varshney R, Tuberosa R (eds) Genomic Assisted Crop Improvement, Vol. 1. Springer, Berlin, pp 351-370
21. Gordon SP, Heisler MG, Reddy GV, Ohno C, Das P, Meyerowitz EM (2007) Pattern formation during de novo assembly of the Arabidopsis shoot meristem. Development 134: 3539-3548
22. 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: genetic variations in hybrid poplars, impact of water deficit and relationships with productivity. Ann Forest Sci 67:1-10
23. Grafi G (2004) How cells dedifferentiate: a lesson from plants. Dev Biol 2: 681-686
24. Gürel E, Wren MJ (1995) In vitro development from leaf explant of sugar beet (Beta vulgarisL). Rhizogenesis and the effect of sequential exposure to auxin and cytokinin. Ann Bot 75: 31-38
25. Hagège D (1996) Habituation in sugarbeet plant cells: permanent stress or antioxidant adaptive strategy? In Vitro Cell Dev Biol 32: 1-5
26. Hall RD, Tjitske R-B, Weyens GJ, Rosquin IJ, Denys PN, Evans IJ, Lathouwers JE, Lefèbvre MP, Dunwell JM van Tunen A, Krens FA (1996) A high efficiency technique for the generation of transgenic sugar beets from stomatal guard cells. Nature Biotechnol 14: 1133-1138
27. Hanania U, Velcheva M, Sahar N, Flaishman M, Or E, Degani O, Perl A (2009) The ubiquitin extension protein S27a is differentially expressed in developing flower organs of Thompson seedless versus Thompson seeded grape isogenic clones. Plant Cell Rep 28: 1033-1042
28. Jacobsen SE, Meyerowitz EM (1997) Hypermethylated SUPERMAN epigenetic alleles in Arabidopsis. Science 277: 1100-1103
29. Jiang M, Zhang Y, Fei J, Chang X, Fan W, Qian X, Zhang T, Lu D (2010) Rapid quantification of DNA methylation by measuring relative peak heights in direct bisulfite-PCR sequencing traces. Lab Investig 90: 282-290
30. Johannes F, Porcher E, Teixeira FK, et al (2009) Assessing the impact of transgenerational epigenetic variation on complex traits. PLoS Genetics 5, e1000530.
31. Kaeppler S, Kaeppler H, Rhee Y (2000) Epigenetic aspects of somaclonal variation in plants. Plant Mol Biol 43: 179-188
32. Kaufmann K, Pajoro A, Angenent GC (2010) Regulation of transcription in plants: mechanisms controlling developmental switches. Nature Reviews Genetics 11: 830-842
33. Krisova K, Fojtova M, Depicker A, Kovarik A (2009) Cell culture-induced gradual and frequent epigenetic reprogramming of invertedly tobacco transgene epialleles. Plant Physiol 149: 1493-1504
34. Laird PW (2003) The power and the promise of DNA methylation markers. Nature 3: 253-266
35. Lauria M, Rossi V (2011) Epigenetic control of gene regulation in plants, BBA- Gene Regulatory Mechanisms. DOI: 10.1016/j.bbagrm.2011.03.002
36. Leakey TI, Zielinski J, Siegfried RN, Siegel ER, Fan CY, Cooney CA (2008) A simple algorithm for quantifying DNA methylation levels on multiple independent CpG sites in bisulfite genomic sequencing electropherograms. Nucl Acids Res 36: e64; DOI: 10.1093/nar/gkn1210
37. Levin R, Gaba V, Tal B, Hirsch S, DeNola D, Vasil IK (1988) Automated plant tissue culture for mass propagation. Biol Tech 6: 1035-1040
38. Li W, Liu H, Cheng ZJ, Su YH, Han HN, Zhang Y, Zhang XS (2011) DNA methylation and histone modifications regulate de novo shoot regeneration in Arabidopsis by modulating WUSCHEL expression and auxin signalling. PLoS Genet 7(8): e1002243. DOI: 10.1371/journal.pgen.1002243
39. Matsuyama T, Kimura M, Koike K, Abe T, Nakano T, Asami T, Ebisuzaki T, Held W, Yoshida S, Nagase H (2003) Global methylation screening in the Arabidopsis thaliana and Mus musculus genome: applications of virtual image restriction landmark genomic scanning (Vi-RLGS). Nucleic Acids Res 31: 4490-4496
40. Miguel C, Marum L (2011) An epigenetic view of plant cells cultured in vitro: somaclonal variation and beyond. J Exp Bot 62: 3713-3725
41. Pischke MS, Huttlin EL, Hegeman AD, Sussman MR (2006) A transcriptome-based characterization of habituation in plant tissue culture. Plant Physiol 140: 1255-1278
42. Rush L, Plass C (2002) Restriction landmark genomic scanning for DNA methylation in cancer: past, present and future applications. Anal Biochem 307: 191-201
43. Schmitz RJ, Schultz MD, Lewsey MG, O'Malley RC, Ulrich MA, Libiger O, Schork NJ, Ecker JR (2011) Transgenerational epigenetic instability is a source of novel methylation variants. Science 334: 369-373
44. Sha AH, Lin XH, Huang JB, Zhang DP (2005) Analysis of DNA methylation related to rice adult plant resistance to bacterial blight based on methylation-sensitive AFLP (MSAP) analysis. Mol Genet and Genomics 273: 484-490
45. Sieburth LE, Meyerowitz EM (1997) Molecular dissection of the AGAMOUS control region shows that cis elements for spatial regulation are located intragenically. Plant Cell 9: 355-365
46. Sugiyama M (1999) Organogenesis in vitro. Curr Opin Plant Biol 2:61-64
47. Takai D, Jones PA (2002) comprehensive analysis of CpG islands in human chromosomes 21 and 22. Proc Natl Acad Sci USA 99: 3740-3745
48. Tanurdzic M, Vaughn M, Jiang H, Lee T-J, Slotkin RK, Sosinski B, Thompson WF, Doerge RW, Martienssen RA (2008) Epigenomic consequences of immortalized plant cell suspension culture. PLoS Biology 6:e302. DOI: 10.1371/journal.pbio.0060302
49. Taylor SM, Jones PA (1979) Multiple new phenotypes induced in 10T1/2 and 3T3 cells treated with 5-azacytidine. Cell 17: 771-779
50. Tessadori F, Chupeau MC, Chupeau Y, Knip M, Germann S, van Driel R, Fransz P, Gaudin V (2007) Large-scale dissociation and sequential reassembly of pericentric heterochromatin in dedifferentiated Arabidopsis cells. J Cell Sci 120: 1200-1208
51. Teyssier E, Bernacchia G, Maury S, How Kit A, Stammitti-Bert L, Rolin D, Gallusci P (2008) Tissue dependent variations of DNA methylation and endoreduplication levels during tomato fruit development and ripening. Planta 228: 391-399
52. Thorpe TA (1980) Organogenesis in vitro: structural, physiological, and biochemical aspects. Int Rev Cytol Suppl 11A: 71-111
53. Trap-Gentil M-V, Hébrard C, Lafon-Placette C, Delaunay A, Hagege 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. J Exp Bot 62: 2585-2597
54. Valledor L, Hasbun R, Meijon M, Rodriguez JL, Santamaria E, Viejo M, Berdasco M, Feito I, Fraga MF, Jesus Canal M, Rodriguez R (2007) Involvement of DNA methylation in tree development and micropropagation. Plant Cell Tissue Organ Cult 91: 75-86
55. Williams L, Zhao J, Morozova N, Li Y, Avivi Y, Grafi G (2003) Chromatin reorganization accompanying cellular dedifferentiation is associated with modifications of histone H3, redistribution of HP1, and activation of E2F-target genes. Dev Dyn 228: 113-120
56. Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ (2007) An "Electronic Fluorescent Pictograph" browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2:e718. DOI: 10.1371/journal.pone.0000718
57. Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan SW-L, Chen H, Henderson IR, Shinn P, Pellegrini M, Jacobsen SE, Ecker JR (2006) Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126: 1189-1201
58. Zhang M, Kimatu JN, Xu K, Liu B (2010) DNA cytosine methylation in plant development. J Genet Genomics 37: 1-12
59. Zhang M, Xu C, von Wettstein D, Liu B (2011) Tissue-specific differences in cytosine methylation and their association with differential gene expression in Sorghum. Plant Physiol 156: 1955-1966
60. Zhao J, Morozova N, Williams L, Libs L, Avivi Y, Grafi G (2001) Two phases of chromatin decondensation during dedifferentiation of plant cells: distinction between competence for cell fate switch and a commitment for S phase. J Biol Chem 276: 22772-22778
61. Zhao XY, Su YH, Cheng ZJ, Zhang XS (2008) Cell fate switch during in vitro plant organogenesis. J Integr Plant Biol 50: 816-824
62. 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 Genet 39: 61-69