Hypomethylation and hypermethylation of the tandem repetitive 5S rRNA genes in Arabidopsis

Plant Journal

Volumn 54, Issue 2, 2008, Pages 299-309

  Vaillant, Isabelle ^a,c   Tutois, Sylvie ^a   Jasencakova, Zuzana ^b,d   Douet, Julien ^a   Schubert, Ingo ^b   Tourmente, Sylvette ^a  

^a Faculté de Médecine   (France)

^b LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

^c UNIVERSITY OF GENEVA   (Switzerland)

^d INSTITUTE OF GENETICS AND BIOPHYSICS ADRIANO BUZZATI TRAVERSO   (Italy)

Author keywords

5S rDNA; Arabidopsis thaliana; Culture conditions; Heterochromatin; Methylation

Indexed keywords

ARABIDOPSIS PROTEIN; RIBOSOME DNA; RNA 5S;

ARABIDOPSIS; ARTICLE; DNA METHYLATION; GENE; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY; TANDEM REPEAT; TIME;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; DNA METHYLATION; DNA, RIBOSOMAL; GENE EXPRESSION REGULATION, PLANT; GENE SILENCING; GENES, PLANT; RNA, RIBOSOMAL, 5S; TANDEM REPEAT SEQUENCES; TIME FACTORS;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 41849148255     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2008.03413.x     Document Type: Article

References (56)

1. AGI (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature, 408, 796 815.
2. Agius, F., Kapoor, A. Zhu, J.K. (2006) Role of the Arabidopsis DNA glycosylase/lyase ROS1 in active DNA demethylation. Proc. Natl Acad. Sci. USA, 103, 11796 11801.
3. Amedeo, P., Habu, Y., Afsar, K., Mittelsten Scheid, O. Paszkowski, J. (2000) Disruption of the plant gene MOM releases transcriptional silencing of methylated genes. Nature, 405, 203 206.
4. Bartee, L., Malagnac, F. Bender, J. (2001) Arabidopsis cmt3 chromomethylase mutations block non-CG methylation and silencing of an endogenous gene. Genes Dev. 15, 1753 1758.
5. Brzeski, J. Jerzmanowski, A. (2003) Deficient in DNA methylation 1 (DDM1) defines a novel family of chromatin-remodeling factors. J. Biol. Chem. 278, 823 828.
6. Campell, B.R., Song, Y., Posch, T.E., Cullis, C.A. Town, C.D. (1992) Sequence and organization of 5S ribosomal RNA-encoding genes of Arabidopsis thaliana. Gene, 112, 225 228.
7. Chan, S.W., Henderson, I.R. Jacobsen, S.E. (2005) Gardening the genome: DNA methylation in Arabidopsis thaliana. Nat. Rev. Genet. 6, 351 360.
8. Chessel, D. (1978) La description non paramétrique de la dispersion spatiale des individus d'une espèce. In Biométrie et Ecologie (Legay, J. M. Tomassone, R., eds). Paris : Société Française de Biométrie, pp. 45 135.
9. Choi, Y., Gehring, M., Johnson, L., Hannon, M., Harada, J.J., Goldberg, R.B., Jacobsen, S.E. Fischer, R.L. (2002) DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in arabidopsis. Cell, 110, 33 42.
10. Cloix, C., Tutois, S., Yukawa, Y., Mathieu, O., Cuvillier, C., Espagnol, M.C., Picard, G. Tourmente, S. (2002) Analysis of the 5S RNA pool in Arabidopsis thaliana: RNAs are heterogeneous and only two of the genomic 5S loci produce mature 5S RNA. Genome Res. 12, 132 144.
11. Doyle (1987) A rapid isolation procedure for small quantities of fresh tissues. Phytochem. Bull. 19, 11 15.
12. Finnegan, E.J. Kovac, K.A. (2000) Plant DNA methyltransferases. Plant Mol. Biol. 43, 189 201.
13. Finnegan, E.J., Genger, R.K., Peacock, W.J. Dennis, E.S. (1998) DNA methylation in Plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 223 247.
14. Fransz, P., Armstrong, S., Alonso-Blanco, C., Fischer, T.C., Torres-Ruiz, R.A. Jones, G. (1998) Cytogenetics for the model system Arabidopsis thaliana. Plant J. 13, 867 876.
15. Fransz, P., De Jong, J.H., Lysak, M., Castiglione, M.R. Schubert, I. (2002) Interphase chromosomes in Arabidopsis are organized as well defined chromocenters from which euchromatin loops emanate. Proc. Natl Acad. Sci. USA, 99, 14584 14589.
16. Fransz, P., ten Hoopen, R. Tessadori, F. (2006) Composition and formation of heterochromatin in Arabidopsis thaliana. Chromosome Res. 14, 71 82.
17. Galaud, J.P., Lareyre, J.J. Boyer, N. (1993) Isolation, sequencing and analysis of the expression of Bryonia calmodulin after mechanical perturbation. Plant Mol. Biol. 23, 839 846.
18. Gehring, M., Huh, J.H., Hsieh, T.F., Penterman, J., Choi, Y., Harada, J.J., Goldberg, R.B. Fischer, R.L. (2006) DEMETER DNA glycosylase establishes MEDEA polycomb gene self-imprinting by allele-specific demethylation. Cell, 124, 495 506.
19. Gong, Z., Morales-Ruiz, T., Ariza, R.R., Roldan-Arjona, T., David, L. Zhu, J.K. (2002) ROS1, a repressor of transcriptional gene silencing in Arabidopsis, encodes a DNA glycosylase/lyase. Cell, 111, 803 814.
20. Grant-Downton, R.T. Dickinson, H.G. (2006) Epigenetics and its implications for plant biology 2. The 'epigenetic epiphany': epigenetics, evolution and beyond. Ann. Bot. 97, 11 27.
21. Haizel, T., Merkle, T., Pay, A., Fejes, E. Nagy, F. (1997) Characterization of proteins that interact with the GTP-bound form of the regulatory GTPase Ran in Arabidopsis. Plant J. 11, 93 103.
22. Jaenisch, R. Bird, A. (2003) Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat. Genet. 33 (Suppl. 245 254.
23. Jeddeloh, J.A., Stokes, T.L. Richards, E.J. (1999) Maintenance of genomic methylation requires a SWI2/SNF2-like protein. Nat. Genet. 22, 94 97.
24. Kapoor, A., Agius, F. Zhu, J.K. (2005) Preventing transcriptional gene silencing by active DNA demethylation. FEBS Lett. 579, 5889 5898.
25. Lindroth, A.M., Cao, X., Jackson, J.P., Zilberman, D., McCallum, C.M., Henikoff, S. Jacobsen, S.E. (2001) Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science, 292, 2077 2080.
26. Lippman, Z., May, B., Yordan, C., Singer, T. Martienssen, R. (2003) Distinct mechanisms determine transposon inheritance and methylation via small interfering RNA and histone modification. PLoS Biol. 1, E67.
27. Luo, S. Preuss, D. (2003) Strand-biased DNA methylation associated with centromeric regions in Arabidopsis. Proc. Natl Acad. Sci. USA, 100, 11133 11138.
28. Madlung, A. Comai, L. (2004) The effect of stress on genome regulation and structure. Ann. Bot. 94, 481 495.
29. Martienssen, R.A. Colot, V. (2001) DNA methylation and epigenetic inheritance in plants and filamentous fungi. Science, 293, 1070 1074.
30. Mathieu, O., Picard, G. Tourmente, S. (2002a) Methylation of a euchromatin-heterochromatin transition region in Arabidopsis thaliana chromosome 5 left arm. Chromosome Res. 10, 455 466.
31. Mathieu, O., Yukawa, Y., Sugiura, M., Picard, G. Tourmente, S. (2002b) 5S rRNA genes expression is not inhibited by DNA methylation in Arabidopsis. Plant J. 29, 313 323.
32. 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.
33. Mathieu, O., Reinders, J., Caikovski, M., Smathajitt, C. Paszkowski, J. (2007) Transgenerational stability of the Arabidopsis epigenome is coordinated by CG methylation. Cell, 130, 851 862.
34. Matzke, M.A. Birchler, J.A. (2005) RNAi-mediated pathways in the nucleus. Nat. Rev. Genet. 6, 24 35.
35. Mittelsten Scheid, O., Probst, A.V., Afsar, K. Paszkowski, J. (2002) Two regulatory levels of transcriptional gene silencing in Arabidopsis. Proc. Natl Acad. Sci. USA, 99, 13659 13662.
36. Murata, M., Heslop-Harrison, J.S. Motoyoshi, F. (1997) Physical mapping of the 5S ribosomal RNA genes in Arabidopsis thaliana by multi-color fluorescence in situ hybridization with cosmid clones. Plant J. 12, 31 37.
37. Onodera, Y., Haag, J.R., Ream, T., Nunes, P.C., Pontes, O. Pikaard, C.S. (2005) Plant nuclear RNA polymerase IV mediates siRNA and DNA methylation-dependent heterochromatin formation. Cell, 120, 613 622.
38. Palmgren, G., Mattsson, O. Okkels, F.T. (1991) Specific levels of DNA methylation in various tissues, cell lines, and cell types of Daucus carota. Plant Physiol. 95, 174 178.
39. Pavet, V., Quintero, C., Cecchini, N.M., Rosa, A.L. Alvarez, M.E. (2006) Arabidopsis displays centromeric DNA hypomethylation and cytological alterations of heterochromatin upon attack by Pseudomonas syringae. Mol. Plant Microbe Interact. 19, 577 587.
40. Penterman, J., Zilberman, D., Huh, J.H., Ballinger, T., Henikoff, S. Fischer, R.L. (2007) DNA demethylation in the Arabidopsis genome. Proc. Natl Acad. Sci. USA, 104, 6752 6757.
41. Rangwala, S.H. Richards, E.J. (2004) The value-added genome: building and maintaining genomic cytosine methylation landscapes. Curr. Opin. Genet. Dev. 14, 686 691.
42. Richards, E.J. (1997) DNA methylation and plant development. Trends Genet. 13, 319 323.
43. Ruiz-Garcia, L., Cervera, M.T. Martinez-Zapater, J.M. (2005) DNA methylation increases throughout Arabidopsis development. Planta, 222, 301 306.
44. Soppe, W.J., Jasencakova, Z., Houben, A., Kakutani, T., Meister, A., Huang, M.S., Jacobsen, S.E., Schubert, I. Fransz, P.F. (2002) DNA methylation controls histone H3 lysine 9 methylation and heterochromatin assembly in Arabidopsis. EMBO J. 21, 6549 6559.
45. Steward, N., Ito, M., Yamaguchi, Y., Koizumi, N. Sano, H. (2002) Periodic DNA methylation in maize nucleosomes and demethylation by environmental stress. J. Biol. Chem. 277, 37741 37746.
46. Tariq, M. Paszkowski, J. (2004) DNA and histone methylation in plants. Trends Genet. 20, 244 251.
47. Tessadori, F., van Driel, R. Fransz, P. (2004) Cytogenetics as a tool to study gene regulation. Trends Plant Sci. 9, 147 153.
48. Tessadori, F., Schulkes, R.K., van Driel, R. Fransz, P. (2007) Light-regulated large-scale reorganization of chromatin during the floral transition in Arabidopsis. Plant J. 50, 848 857.
49. Tompa, R., McCallum, C.M., Delrow, J., Henikoff, J.G., van Steensel, B. Henikoff, S. (2002) Genome-wide profiling of DNA methylation reveals transposon targets of CHROMOMETHYLASE3. Curr. Biol. 12, 65 68.
50. Tran, R.K., Zilberman, D., de Bustos, C. et al. (2005) Chromatin and siRNA pathways cooperate to maintain DNA methylation of small transposable elements in Arabidopsis. Genome Biol. 6, R90.
51. Tutois, S.C.C., Mathieu, O., Cuvillier, C. Tourmente, S. (2002) Analysis of 5S rDNA Loci among Arabidopsis ecotypes and subspecies. Genome Lett. 1, 115 122.
52. Vaillant, I., Schubert, I., Tourmente, S. Mathieu, O. (2006) MOM1 mediates DNA-methylation-independent silencing of repetitive sequences in Arabidopsis. EMBO Rep. 7, 1273 1278.
53. Vaillant, I., Tutois, S., Cuvillier, C., Schubert, I. Tourmente, S. (2007) Regulation of Arabidopsis thaliana 5S rRNA genes. Plant Cell Physiol. 48, 745 752.
54. Zhang, X., Yazaki, J., Sundaresan, A. et al. (2006) Genome-wide high-resolution mapping and functional analysis of DNA methylation in arabidopsis. Cell, 126, 1189 1201.
55. Zhu, J., Kapoor, A., Sridhar, V.V., Agius, F. Zhu, J.K. (2007) The DNA glycosylase/lyase ROS1 functions in pruning DNA methylation patterns in Arabidopsis. Curr. Biol. 17, 54 59.
56. Zilberman, D. Henikoff, S. (2004) Silencing of transposons in plant genomes: kick them when they're down. Genome Biol. 5, 249.