Dedifferentiation of tobacco cells is associated with ribosomal RNA gene hypomethylation, increased transcription, and chromatin alterations

Plant Physiology

Volumn 139, Issue 1, 2005, Pages 275-286

  Koukalova, Blazena ^a   Fojtova, Miloslava ^a   Lim, Kar Yoong ^b   Fulnecek, Jaroslav ^a   Leitch, Andrew Rowland ^b   Kovarik, Ales ^a  

^a INSTITUTE OF BIOPHYSICS   (Czech Republic)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GENES; RNA; TOBACCO;

HYBRIDIZATION ANALYSIS; MERISTEMATIC ROOT-TIP CELLS; RIBOSOMAL DNA (RDNA);

CELLS;

CELLS; GENES; NUCLEIC ACIDS; TOBACCO;

NICOTIANA TABACUM;

MESSENGER RNA; RIBOSOME RNA;

ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CHEMISTRY; CHROMATIN; CYTOLOGY; DNA METHYLATION; FLUORESCENCE IN SITU HYBRIDIZATION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; INTERPHASE; METABOLISM; PLANT LEAF; PLANT ROOT; REGENERATION; TOBACCO;

CELL DIFFERENTIATION; CELLS, CULTURED; CHROMATIN; DNA METHYLATION; GENE EXPRESSION REGULATION, PLANT; IN SITU HYBRIDIZATION, FLUORESCENCE; INTERPHASE; PLANT LEAVES; PLANT ROOTS; REGENERATION; RNA, MESSENGER; RNA, RIBOSOMAL; TOBACCO; TRANSCRIPTION, GENETIC;

EID: 33644788375     PISSN: 00320889     EISSN: None     Source Type: Journal    
DOI: 10.1104/pp.105.061788     Document Type: Review

References (58)

1. Amado L, Abranches R, Neves N, Viegas W (1997) Development-dependent inheritance of 5-azacytidine-induced epimutations in triticale: analysis of rDNA expression patterns. Chromosome Res 5: 445-450
2. Anderson S, Lewis-Smith AC, Smith SM (1990) Methylation of ribosomal RNA genes in Petunia hybrida plants, callus cultures and regenerated shoots. Plant Cell Rep 8: 554-557
3. Arnholdt-Schmitt B (2004) Stress-induced reprogramming. A role for global genome regulation? Plant Physiol 136: 2579-2536
4. Arnholdt-Schmitt B, Hesterich S, Neumann K-H (1995) Physiological aspects of genome variability in tissue culture, I. Growth phase-dependent differential DNA methylation of the carrot genome (Daucus carrota L.) during primary culture. Theor Appl Genet 91: 809-815
5. Avivi Y, Morad V, Ben-Meir H, Zhao J, Kashkush K, Tzfira T, Citovsky V, Grafi G (2004) Reorganization of specific chromosomal domains and activation of silent genes in plant cells acquiring pluripotentiality. Dev Dyn 230: 12-22
6. Brock GJR, Bird A (1997) Mosaic methylation of the repeat units of the human ribosomal RNA genes. Hum Mol Genet 6: 451-456
7. Castilho A, Neves N, Rufini-Castiglione M, Viegas W, Heslop-Harrison JS (1999) 5-Methylcytosine distribution and genome organization in triticale before and after treatment with 5-azacytidine. J Cell Sci 112: 4397-4404
8. Cerdido A, Medina FJ (1995) Subnucleolar location of fibrillarin and variation in its levels during the cell cycle and during differentiation of plant cells. Chromosoma 103: 625-634
9. Chen ZJ, Pikaard CS (1997) Epigenetic silencing of RNA polymerase I transcription: a role for DNA methylation and histone modification in nucleolar dominance. Genes Dev 11: 2124-2136
10. Fan H, Yakura K, Miyanishi M, Sugita M, Sugiura M (1995) In vitro transcription of plant RNA polymerase I-dependent rRNA genes is species-specific. Plant J 8: 295-293
11. Finnegan EJ, Kovac KA (2000) Plant DNA methyltransferases. Plant Mol Biol 43: 139-201
12. Flavell RB, O'Dell M, Thompson WF (1988) Regulation of cytosine methylation in ribosomal DNA and nucleolus organizer expression in wheat. J Mol Biol 204: 523-534
13. Fojtova M, Van Houdt H, Depicker A, Kovarik A (2003) Epigenetic switch from posttranscriptional to transcriptional silencing is correlated with promoter hypermethylation. Plant Physiol 133: 1240-1250
14. Fulnecek J, Matyasek R, Kovarik A, Bezdek M (1998) Mapping of 5-methylcytosine residues in Nicotiana tabacum 5S rRNA genes by genomic sequencing. Mol Gen Genet 259: 133-141
15. Gaudino RJ, Pikaard CS (1997) Cytokinin induction of RNA polymerase I transcription in Arabidopsis thaliana. J Biol Chem 272: 6799-6804
16. Glyn MC, Egertova M, Gazdova B, Kovarik A, Bezdek M, Leitch AR (1995) The influence of 5-azacytidine on the condensation of the short arm of rye chromosome 1R in Triticum aestivum L. root tip meristematic nuclei. Chromosoma 106: 485-492
17. Goodspeed TH (1954) The Genus Nicotiana, Vol 16. Chronica Botanica, Waltham, MA
18. Grafi G (2004) How cells differentiate: lessons from plants. Dev Biol 268: 1-6
19. Hasterok R, Maluszynska J (2000) Different rRNA gene expression in primary and adventitious roots of Allium cepa L. Folia Histochem Cytobiol 38: 131-134
20. Hemleben V, Zentgraf U (1994) Structural organisation and regulation of transcription by RNA polymerase I of plant nuclear ribosomal genes. In L Nover, ed, Results and Problems in Cell Differentiation 20: Plant Promoters and Transcription Factors. Springer-Verlag, Berlin/Heidelberg, pp 3-24
21. Hodurkova J, Vyskot B (2003) Histone H4 acetylation patterns during seed germination and early plant development. Biol Plant (Prague) 46: 23-23
22. Jaligot E, Rival A, Beule T, Dussert S, Verdeil JL (2000) Somaclonal variation in oil palm (Elaesis guineensis Jacg.): the DNA methylation hypothesis. Plant Cell Rep 19: 634-690
23. Jupe ER, Zimmer EA (1990) Unmethylated regions in the intergenic spacer of maize and teosinte ribosomal RNA genes. Plant Mol Biol 14: 333-347
24. Kaeppler SM, Kaeppler HF, Rhee Y (2000) Epigenetic aspects of somaclonal variation in plants. Plant Mol Biol 43: 179-133
25. Kenton A, Parokonny AS, Gleba YY, Bennett MD (1993) Characterization of the Nicotiana tabacum L. genome by molecular cytogenetics. Mol Gen Genet 240: 159-169
26. Kiss T, Szkukalek A, Solymosy F (1989) Nucleotide sequence of a 17S (18S) rRNA gene from tomato. Nucleic Acids Res 17: 2127
27. Komarova NY, Grabe T, Huigen DJ, Hemleben V, Volkov RA (2004) Organization, differential expression and methylation of rDNA in artificial Solanum allopolyploids. Plant Mol Biol 56: 439-463
28. Kovarik A, Koukalova B, Bezdek M, Opatmy Z (1997) Hypermethylation of tobacco heterochromatic loci in response to osmotic stress. Theor Appl Genet 95: 301-306
29. Kovarik A, Koukalova B, Lim KY, Matyasek R, Lichtenstein CP, Leitch AR, Bezdek M (2000) Comparative analysis of DNA methylation in tobacco heterochromatic sequences. Chromosome Res 8: 527-541
30. Kovarik A, Matyasek R, Lim KY, Skalická K, Koukalova B, Knapp S, Chase M, Leitch AR (2004) Concerted evolution of 18-5.8-26S rDNA repeats in Nicotiana allotetraploids. Biol J Linn Soc 82: 615-625
31. Kovarik A, Pires JC, Leitch AR, Lim KY, Sherwood A, Matyasek R, Rocca J, Soltis DE, Soltis PS (2005) Rapid concerted evolution of nuclear ribosomal DNA in two allopolyploids of recent and recurrent origin. Genetics 169: 931-944
32. Labra M, Ghiani A, Citterio S, Sgorbati S, Sala F, Vannini C, Ruffini-Castiglione M, Bracale M (2002) Analysis of cytosine methylation pattern in response to water deficit in pea root tips. Plant Biol 4: 694-699
33. Lawrence RJ, Earley K, Pontes O, Silva M, Chen ZJ, Neves N, Viegas W, Pikaard CS (2004) A concerted DNA methylation/histone methylation switch regulates rRNA gene dosage control and nucleolar dominance. Mol Cell 13: 599-609
34. Leitch AR, Schwarzacher T, Wang ML, Leitch IJ, Surlan-Momirovich G, Moore G, Heslop-Harrison JS (1993) Molecular cytogenetic analysis of repeated sequences in a long term wheat suspension culture. Plant Cell Tissue Organ Cult 33: 287-296
35. Lim KY, Kovarik A, Matyasek R, Bezdek M, Lichtenstein CP, Leitch AR (2000) Gene conversion of ribosomal DNA in Nicotiana tabacum is associated with undermethylated, decondensed and probably active gene units. Chromosoma 109: 161-172
36. Lim KY, Skalická K, Koukalova B, Volkov RA, Matyasek R, Hemleben V, Leitch AR, Kovarik A (2004) Dynamic changes in the distribution of a satellite homologous to intergenic 26-18S rDNA spacer in the evolution of Nicotiana. Genetics 166: 1935-1946
37. Mathieu O, Jasencakova Z, Vaillant I, Gendrel A-V, Colot V, Schubert I, Tourmente S (2003) Changes in 5S rDNA chromatin organization and transcription during heterochromatin establishment in Arabidopsis. Plant Cell 15: 2929-2939
38. Mathieu O, Picard G, Tourmente S (2002) Methylation of an euchromatin-heterochromatin transition region in Arabidopsis thaliana chromosome 5 left arm. Chromosome Res 10: 455-466
39. Mitsuhara I, Shirasawa-Seo N, Iwai T, Nakamura S, Honkura R, Ohashi Y (2002) Release from post-transcriptional gene silencing by cell proliferation in transgenic tobacco plants: possible mechanism for non-inheritance of the silencing. Genetics 160: 343-352
40. Moscone EA, Matzke MA, Matzke AJ (1996) The use of combined FISH/GISH in conjunction with DAPI counterstaining to identify chromosomes containing transgene inserts in amphidiploid tobacco. Chromosoma 105: 231-236
41. Olhoft PM, Phillips RL (1999) Genetic and epigenetic instability in tissue culture and regenerated progenies. In HR Lerner, ed, Plant Responses to Environmental Stresses: From Phytohormones to Genome Reorganization. Marcel Dekker, New York, pp 111-143
42. Pikaard CS (2000) The epigenetics of nucleolar dominance. Trends Genet 16: 495-500
43. Reichheld JP, Chaubet N, Shen WH, Renaudin JP, Gigot C (1996) Multiple A-type cyclins express sequentially during the cell cycle in Nicotiana tabacum BY2 cells. Proc Natl Acad Sci USA 93: 13819-13824
44. Santoro R, Grummt I (2001) Molecular mechanisms mediating methylation-dependent silencing of ribosomal gene transcription. Mol Cell 8: 719-725
45. Sardana R, O'Dell M, Flavell R (1993) Correlation between the size of the intergenic regulatory region, the status of cytosine methylation of rRNA genes and nucleolar expression in wheat. Mol Gen Genet 236: 155-162
46. Skalická K, Lim KY, Matyásek R, Koukalová B, Leitch AR, Kovarík A (2003) Rapid evolution of parental rDNA in a synthetic tobacco allotetraploid line. Am J Bot 90: 988-996
47. Smulders MJM, Rus-Kortekaas W, Vosman B (1995) Tissue culture-induced DNA methylation polymorphisms in repetitive DNA of tomato calli and regenerated plants. Theor Appl Genet 91: 1257-1264
48. Soppe WJ, Jasencakova Z, Houben A, Kakutani T, Meister A, Huang MS, Jacobsen SE, Schubert I, Fransz PF (2002) DNA methylation controls histone H3 lysine 9 methylation and heterochromatin assembly in Arabidopsis. EMBO J 21: 6549-6559
49. Tariq M, Saze H, Probst AV, Lichota J, Habu Y, Paszkowski J (2003) Erasure of CpG methylation in Arabidopsis alters patterns of histone H3 methylation in heterochromatin. Proc Natl Acad Sci USA 100: 8823-8827
50. Torres-Ruiz RA, Hemleben V (1994) Pattern and degree of methylation in ribosomal RNA genes of Cucurbita pepo L. Plant Mol Biol 26: 1167-1179
51. van Blokland R, van der Geest N, Mol JN, Kooter JM (1994) Transgene-mediated suppression of chalcone synthase expression in Petunia hybrida results from an increase in RNA turnover. Plant J 6: 861-877
52. Van Houdt H, Kovarik A, Van Montagu M, Depicker A (2000) Cross-talk between posttranscriptionally silenced neomycin phosphotransferase II transgenes. FEBS Lett 467: 41-46
53. Viera R, Queiroz A, Morais L, Barao A, Mello-Sampavo T, Viegas WS (1990) 1R chromosome nucleolus organiser region activation by 5-azacytidine in wheat × rye hybrids. Genome 33: 707-712
54. Volkov RA, Borisjuk NV, Panchuk II, Schweizer D, Hemleben V (1999) Elimination and rearrangement of parental rDNA in the allotetraploid Nicotiana tabacum. Mol Biol Evol 16: 311-320
55. Vyskot B, Gazdova B, Siroky J (1993) Methylation patterns of two repetitive DNA sequences in tobacco tissue cultures and their regenerants. Biol Plant (Prague) 35: 321-327
56. Vyskot B, Koukalova B, Kovarik A, Sachambula L, Reynolds D, Bezdek M (1995) Meiotic transmission of a hypomethylated repetitive DNA family in tobacco. Theor Appl Genet 91: 659-664
57. Watson JC, Kaufman LS, Thompson WF (1987) Developmental regulation of cytosine methylation in the nuclear ribosomal RNA genes of Pisum sativum. J Mol Biol 193: 15-26
58. 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