Advertisement

Plant Molecular Biology

, Volume 43, Issue 2–3, pp 203–220 | Cite as

RNA-directed DNA methylation

  • Michael Wassenegger
Article

Abstract

RNA-DNA interactions can serve as a signal that triggers de novo DNA methylation in plants. As yet, this RNA-directed DNA methylation mechanism merely targets transgenes, but it appears likely that methylation of some endogenous sequences is also directed by RNA. RNA-directed methylation of cytosine residues specifically occurs along the DNA regions that are complementary to the directing RNA pointing to the formation of a putative RNA-DNA duplex. Dense methylation patterns and the methylation of cytosine residues at symmetric and asymmetric sites are detectable on both DNA strands within these regions. Methylation progressively decreases in the sequences adjacent to the putative RNA-DNA duplex. The extreme sensitivity of RNA-directed DNA methylation was demonstrated by analysing a short 30 bp DNA region that was complementary to the targeting RNA. Association of RNA-directed DNA methylation with homology-dependent gene silencing indicated that the methylation-directing RNA molecules may be double-stranded or may contain double-stranded regions. Whereas the function of DNA methylation in transcriptional gene silencing is nearly understood, its role in post-transcriptional gene silencing is still under discussion. In mammals, X-chromosome inactivation and genomic imprinting are associated with DNA methylation but how methylation is initiated is unclear. The observation of a correlation between specific antisense RNAs and transcriptional and post-transcriptional gene silencing may indicate that RNA-directed DNA methylation is involved in epigenetic gene regulation throughout eukaryotes.

5-methylcytosine RNA-directed DNA methylation RNA-DNA hybrid RNA-directed RNA polymerase viroids 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Alvarado, A.S. and Newmark, P.A. 1999. Double-stranded RNA specifically disrupts gene expression during planarian regeneration. Proc. Natl. Acad. Sci. USA 96: 5049–5054.PubMedGoogle Scholar
  2. Amasino, R.M., Powell, A.L.T. and Gordon, M.P. 1984. Changes in T-DNA methylation and expression are associated with phenotypic variation and plant regeneration in a crown gall tumor line. Mol. Gen. Genet. 197: 437–446.PubMedGoogle Scholar
  3. Barlow, D.P. 1997. Competition: a common motif for the imprinting mechanism. EMBO J. 16: 6899–6905.PubMedGoogle Scholar
  4. Barry, C., Faugeron, G. and Rossignol, J.-L. 1993. Methylation induced premeiotically in Ascobolus: coextension with DNA repeat length and effect on transcription elongation. Proc. Natl. Acad. Sci. USA 90: 4557–4561.PubMedGoogle Scholar
  5. Baulcombe, D.C. 1996. RNA as a target and an initiator of posttranscriptional gene silencing in transgenic plants. Plant Mol. Biol. 32: 79–88.PubMedGoogle Scholar
  6. Baulcombe, D.C. and English, J.J. 1996. Ectopic pairing of homologous DNA and post-transcriptional gene silencing in transgenic plants. Curr. Opin. Biotechnol. 7: 173–180.Google Scholar
  7. Bender, J. 1998. Cytosine methylation of repeated sequences in eukaryotes: the role of DNA pairing. Trends Biochem. Sci. 23: 252–256.PubMedGoogle Scholar
  8. Bestor, T.H. and Tycko, B. 1996. Creation of genomic methylation patterns. Nature Genet. 12: 363–367.PubMedGoogle Scholar
  9. Brigneti, G., Voinnet, O., Li, W.X., Ji, L.H., Ding, S.W. and Baulcombe, D.C. 1998. Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana. EMBO J. 17: 6739–6746.PubMedGoogle Scholar
  10. Busslinger, M., Hurst, J. and Flavell, R.A. 1983. DNA methylation and the regulation of the globin gene expression. Cell 34: 197–206.PubMedGoogle Scholar
  11. Clark, S.J., Harrison, J., Paul, C.L. and Frommer, M. 1994. High sensitivity mapping of methylated cytosines. Nucl. Acids Res. 22: 2990–2997.PubMedGoogle Scholar
  12. Clemson, C.M., McNeil, J.A., Willard, H.F. and Lawrence, J.B. 1996. XIST RNA paints the inactive X chromosome at interphase: evidence for a novel RNA involved in nuclear chromosome structure. J. Cell Biol. 132: 259–275.PubMedGoogle Scholar
  13. Cogoni, C., Irelan, J.T., Schumacher, M., Schmidhauser, T.J., Selker, E.U. and Macino, G. 1996. Transgene silencing of the al-1 gene in vegetative cells of Neurospora is mediated by a cytoplasmic effector and does not depend on DNA-DNA interactions or DNA methylation. EMBO J. 15: 3153–3163.PubMedGoogle Scholar
  14. Colot, V., Maloisel, L. and Rossignol, J.L. 1996. Interchromosomal transfer of epigenetic states in Ascobulus: transfer of DNA methylation is mechanistically related to homologous recombination. Cell 86: 855–864.PubMedGoogle Scholar
  15. Diéguez, M.J., Vaucheret, H., Paszkowski, J. and Mittelsten Scheid, O. 1998. Cytosine methylation at CG and CNG sites is not a prerequisite for the initiation of transcriptional gene silencing in plants, but is required for its maintenance. Mol. Gen. Genet. 259: 207–215.PubMedGoogle Scholar
  16. Elmayan, T. and Vaucheret, H. 1996. Expression of single copies of a strongly expressed 35S transgene can be silenced posttranscriptionally. Plant J. 9: 787–797.Google Scholar
  17. Elmayan, T., Balzergue, S., Beon, F., Bourdon, V., Daubremet, J., Guenet, Y., Mourrain, P., Palauqui, J.C., Vernhettes, S., Vialle, T., Wostrikoff, K. and Vaucheret, H. 1998. Arabidopsis mutants impaired in cosuppression. Plant Cell 10: 1747–1757.PubMedGoogle Scholar
  18. Finnegan, E.J., Genger, R.K., Peacock, W.J. and Dennis, E.S. 1998. DNA methylation in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49: 223–247.PubMedGoogle Scholar
  19. Fire, A. 1999. RNA-triggered gene silencing. Trends Genet. 15: 358–363.PubMedGoogle Scholar
  20. Fire, A., Xu, S.Q., Montgomery, M.K., Kostas, S.A., Driver, S.E. and Mello, C.C. 1998. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391: 806–811.PubMedGoogle Scholar
  21. Frommer, M., McDonald, L.E., Millar, D.S., Collins, C.M., Watt, F., Grigg, G.W., Molloy, P.L. and Paul, C.L. 1992. A genomic sequencing protocol that yields a positive display of 5–methylcytosine residues in individual DNA strands. Proc. Natl. Acad. Sci. USA 89: 1827–1831.PubMedGoogle Scholar
  22. Goerz, A., Schaefer, W., Hirasawa, E. and Kahl, G. 1988. Constitutive and light-induced DNase I hypersensitive sites in the rbcS genes of pea (Pisum sativum). Plant Mol. Biol. 11: 561–573.Google Scholar
  23. Grunstein, M. 1997. Histone acetylation in chromatin structure and transcription. Nature 389: 349–352.PubMedGoogle Scholar
  24. Harders, J., Lukás, N., Robert-Nicoud, M., Jovin, T.M. and Riesner, D. 1989. Imaging of viroids in nuclei from tomato leaf tissue by in situ hybridization and confocal laser scanning. EMBO J. 8: 3941–3949.PubMedGoogle Scholar
  25. Henikoff, S. 1990. Position-effect variegation after 60 years. Trends Genet. 6: 422–426.PubMedGoogle Scholar
  26. Hohn, T., Corsten, S., Rieke, S., Müller, M. and Rothnie, H. 1996. Methylation of coding region alone inhibits gene expression in plant protoplasts. Proc. Natl. Acad. Sci. USA 93: 8334–8339.PubMedGoogle Scholar
  27. Hu, J.F., Balaguru, K.A., Ivaturi, R.D., Oruganti, H., Li, T., Nguyen, B.T., Vu, T.H. and Hoffman, A.R. 1999. Lack of reciprocal genomic imprinting of sense and antisense RNA of mouse insulin-like growth factor II receptor in the central nervous system. Biochem. Biophys. Res. Comm. 257: 604–608.PubMedGoogle Scholar
  28. Ingelbrecht, I., Van Houdt, H., Van Montagu, M. and Depicker, A. 1994. Posttranscriptional silencing of reporter transgenes in tobacco correlates with DNA methylation. Proc. Natl. Acad. Sci. USA 91: 10502–10506.PubMedGoogle Scholar
  29. Jacobs, J.J.M.R., Sanders, M., Bots, M., Andriessen, M., van Eldik, G.J., Litiere, K., Van Montagu, M. and Cornelissen, M. 1999. Sequences throughout the basic β-1,3–glucanase mRNA coding region are targets for homology dependent post-transcriptional gene silencing. Plant J. 20: 143–152.PubMedGoogle Scholar
  30. Jensen, S., Gassama, M.P. and Heidmann, T. 1999. Taming of transposable elements by homology-dependent gene silencing. Nature Genet. 21: 209–212.PubMedGoogle Scholar
  31. Jirtle, R.L. 1999. Genomic imprinting and cancer. Exp. Cell Res. 248: 18–24.PubMedGoogle Scholar
  32. Jones, A.L., Thomas, C.L. and Maule, A.J. 1998a. De novo methylation and co-suppression induced by a cytoplasmically replicating plant RNA virus. EMBO J. 17: 6385–6393.PubMedGoogle Scholar
  33. Jones, P.L., Veenstra, G.J.C., Wade, P.A., Vermaak, D., Kass, S.U., Landsberger, N., Strouboulis, J. and Wolffe, A.P. 1998b. Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nature Genet. 19: 187–191.PubMedGoogle Scholar
  34. Jong, M.T.C., Gray, T.A., Ji, Y.G., Glenn, C.C., Saitoh, S., Driscoll, D.J. and Nicholls, R.D. 1999. A novel imprinted gene, encoding a RING zinc-finger protein, and overlapping antisense transcript in the Prader-Willi syndrome critical region. Hum. Mol. Genet. 8: 783–793.PubMedGoogle Scholar
  35. Jorgensen, R.A., Que, Q. and Stam, M. 1999. Do unintended antisense transcripts contribute to sense cosuppression in plants? Trends Genet 15: 11–12.PubMedGoogle Scholar
  36. Jost, J.P. and Bruhat, A. 1997. The formation of DNA methylation patterns and the silencing of genes. Prog. Nucl. Acid Res. Mol. Biol. 57: 217–248.Google Scholar
  37. Kass, S.U., Landsberger, N. and Wolffe, A.P. 1997. DNA methylation directs a time-dependent repression of transcription initiation. Curr. Biol. 7: 157–165.PubMedGoogle Scholar
  38. Kennerdell, J.R. and Carthew, R.W. 1998. Use of dsRNA-mediated genetic interference to demonstrate that frizzled and frizzled 2 act in the wingless pathway. Cell 95: 1017–1026.PubMedGoogle Scholar
  39. Kooter, J.M., Matzke, M.A. and Meyer, P. 1999. Listening to the silent genes: transgene silencing, gene regulation and pathogen control. Trends Plant Sci. 4: 340–347.PubMedGoogle Scholar
  40. Korneev, S.A., Park, J.H. and O'Shea, M. 1999. Neuronal expression of neural nitric oxide synthase (nNOS) protein is suppressed by an antisense RNA transcribed from an NOS pseudogene. J. Neurosci. 19: 7711–7720.PubMedGoogle Scholar
  41. Kumpatla, S.P., Chandrasekharan, M.B., Iyer, L.M., Li, G.F. and Hall, T.C. 1998. Genome intruder scanning and modulation systems and transgene silencing. Trends Plant Sci. 3: 97–104.Google Scholar
  42. Lee, J.T. and Lu, N. 1999. Targeted mutagenesis of Tsix leads to nonrandom X inactivation. Cell 99: 47–57.PubMedGoogle Scholar
  43. Lee, J.T., Davidow, L.S. and Warshawsky, D. 1999a. Tsix, a gene antisense to Xist at the X-inactivation centre. Nature Genet. 21: 400–404.PubMedGoogle Scholar
  44. Lee, M.P., DeBaun, M.R., Mitsuya, K., Galonek, H.L., Brandenburg, S., Oshimura, M. and Feinberg, A.P. 1999b. Loss of imprinting of a paternally expressed transcript, with antisense orientation to KvLQT1, occurs frequently in Beckwith-Wiedemann syndrome and is independent of insulin-like growth factor II imprinting. Proc. Natl. Acad. Sci. USA 96: 5203–5208.PubMedGoogle Scholar
  45. Lewis, J.D., Meehan, R.R., Henzel, W.J., Maurer-Fogy, I., Jeppesen, P., Klein, F. and Bird, A. 1992. Purification, sequence, and cellular localization of a novel chromosomal protein that binds to methylated DNA. Cell 69: 905–914.PubMedGoogle Scholar
  46. Li, E. 1999. The mojo of methylation. Nature Genet. 23: 5–6.PubMedGoogle Scholar
  47. Loss, P., Schmitz, M., Steger, G. and Riesner, D. 1991. Formation of a thermodynamically metastable structure containing hairpin II is critical for infectivity of potato spindle tuber viroid RNA. EMBO J. 10: 719–727.PubMedGoogle Scholar
  48. Luff, B., Pawlowski, L. and Bender, J. 1999. An inverted repeat triggers cytosine methylation of identical sequences in Arabidopsis. Mol. Cell 3: 505–511.CrossRefPubMedGoogle Scholar
  49. Malagnac, F., Wendel, B., Goyon, C., Faugeron, G., Zickler, D., Rossignol, J.L., Noyer Weidner, M., Vollmayr, P., Trautner, T.A. and Walter, J. 1997. A gene essential for de novo methylation and development in ascobolus reveals a novel type of eukaryotic DNA methyltransferase structure. Cell 91: 281–290.PubMedGoogle Scholar
  50. Matzke, M.A. and Matzke, A.J.M. 1995. How and why do plants inactivate homologous (trans)genes? Plant Physiol. 107: 679–685.PubMedGoogle Scholar
  51. Matzke, M.A. and Matzke, A.J.M. 1998a. Epigenetic silencing of plant transgenes as a consequence of diverse cellular defence responses. Cell. Mol. Life Sci. 54: 94–103.PubMedGoogle Scholar
  52. Matzke, A.J.M. and Matzke, M.A. 1998b. Position effects and epigenetic silencing of plant transgenes. Curr. Opin. Plant Biol. 1: 142–148.PubMedGoogle Scholar
  53. Matzke, A.J.M., Neuhuber, F., Park, Y.-D., Ambros, P.F. and Matzke, M.A. 1994. Homology-dependent gene silencing in transgenic plants: epistatic silencing loci contain multiple copies of methylated transgenes. Mol. Gen. Genet. 244: 219–229.PubMedGoogle Scholar
  54. McDonald, L.E., Paterson, C.A. and Kay, G.F. 1998. Bisulfite genomic sequencing-derived methylation profile of the Xist gene throughout early mouse development. Genomics 54: 379–386.PubMedGoogle Scholar
  55. Mette, F., van der Winden, J., Matzke, M.A. and Matzke, A.J.M. 1999. Production of aberrant promoter transcripts contributes to methylation and silencing of unlinked homologous promoters in trans. EMBO J. 18: 241–248.PubMedGoogle Scholar
  56. Metzlaff, M., O'Dell, M., Cluster, P.D. and Flavell, R.B. 1997. RNA-mediated degradation and chalcone synthase A silencing in Petunia. Cell 88: 845–854.PubMedGoogle Scholar
  57. Mise, N., Goto, Y., Nakajima, N. and Takagi, N. 1999. Molecular cloning of antisense transcripts of the mouse Xist gene. Biochem. Biophys. Res. Comm 258: 537–541.PubMedGoogle Scholar
  58. Misquitta, L. and Paterson, B.M. 1999. Targeted disruption of gene function in Drosophila by RNA interference (RNA-i): a role for nautilus in embryonic somatic muscle formation. Proc. Natl. Acad. Sci. USA 96: 1451–1456.PubMedGoogle Scholar
  59. Mitsuya, K., Meguro, M., Lee, M.P., Katoh, M., Schulz, T.C., Kugoh, H., Yoshida, M.A., Niikawa, N., Feinberg, A.P. and Oshimura, M. 1999. LIT1, an imprinted antisense RNA in the human KvLQT1 locus identified by screening for differentially expressed transcripts using monochromosomal hybrids. Hum. Mol. Genet. 8: 1209–1217.PubMedGoogle Scholar
  60. Montgomery, M.K. and Fire, A. 1998. Double-stranded RNA as a mediator in sequence-specific genetic silencing and cosuppression. Trends Genet. 14: 255–258.PubMedGoogle Scholar
  61. Moore, T., Constancia, M., Zubair, M., Bailleul, B., Feil, R., Sasaki, H. and Reik, A. 1997. Multiple imprinted sense and antisense transcripts, differential methylation and tandem repeats in a putative imprinting control region upstream of mouse Igf2. Proc. Natl. Acad. Sci. USA 94: 12509–12514.PubMedGoogle Scholar
  62. Nan, X.S., Ng, H.H., Johnson, C.A., Laherty, C.D., Turner, B.M., Eisenman, R.N. and Bird, A. 1998. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393: 386–389.PubMedGoogle Scholar
  63. Ng, H.H., Zhang, Y., Hendrich, B., Johnson, C.A., Turner, B.M., Erdjument-Bromage, H., Tempst, P., Reinberg, D. and Bird, A. 1991. MBD2 is a transcriptional repressor belonging to the MeCP1 histone deacetylase complex. Nature Genet. 23: 58–61.Google Scholar
  64. Ngô, H., T schudi, C., Gull, K. and Ullu, E. 1998. Double-stranded RNA induces mRNA degradation in Trypanosoma brucei. Proc. Natl. Acad. Sci. USA 95: 14687–14692.PubMedGoogle Scholar
  65. Nick, H., Bowen, B., Ferl, R.J. and Gilbert, W. 1986. Detection of cytosine methylation in the maize alcohol dehydrogenase gene by genomic sequencing. Nature 319: 243–246.Google Scholar
  66. Norris, D.P., Patel, D., Kay, G.F., Penny, G.D., Brockdorff, N., Sheardown, S.A. and Rastan, S. 1994. Evidence that random and imprinted Xist expression is controlled by preemptive methylation. Cell 77: 41–51.PubMedGoogle Scholar
  67. Palauqui, J.C. and Balzergue, S. 1999. Activation of systemic silencing by localised introduction of DNA. Curr. Biol. 9: 59–66.PubMedGoogle Scholar
  68. Palauqui, J.C., Elmayan, T., Pollien, J.M. and Vaucheret, H. 1997. Systemic acquired silencing: transgene-specific posttranscriptional silencing is transmitted by grafting from silenced stocks to non-silenced scions. EMBO J. 16: 4738–4745.PubMedGoogle Scholar
  69. Palladino, F. and Gasser, S. 1994. Telomeric maintenance and gene repression: a common end? Curr. Opin. Cell Biol. 6: 373–379.PubMedGoogle Scholar
  70. Paro, R. 1993. Mechanisms of heritable gene repression during development of Drosophila. Curr. Opin. Cell Biol. 5: 999–1005.PubMedGoogle Scholar
  71. Pélissier, T. and Wassenegger, M. 2000. A DNA target of 30 bp is sufficient for RNA-directed DNA methylation. RNA 6: 55–65PubMedGoogle Scholar
  72. Pélissier, T., Thalmeir, S., Kempe, D., Sänger, H.L. and Wassenegger, M. 1999. Heavy de novo methylation at symmetrical and non-symmetrical sites is a hallmark of RNA-directed DNA methylation. Nucl. Acids Res. 27: 1625–1634.PubMedGoogle Scholar
  73. Que, Q., Wang, H.Y., English, J.J. and Jorgensen, R.A. 1997. The frequency and degree of cosuppression by sense chalcone synthase transgenes are dependent on transgene promoter strength and are reduced by premature nonsense codons in the transgene coding sequence. Plant Cell 9: 1357–1368.PubMedGoogle Scholar
  74. Reik, W. and Constancia, M. 1997. Making sense or antisense? Nature 389: 669–671.PubMedGoogle Scholar
  75. Rivier, D.H. and Pillus, L. 1994. Silencing speaks up. Cell 76: 963–966.PubMedGoogle Scholar
  76. Roth, S.Y. 1995. Chromatin-mediated transcriptional repression in yeast. Curr. Opin. Gen. Dev. 5: 168–173.Google Scholar
  77. Rougeulle, C., Cardoso, C., Fontés, M., Colleaux, L. and Lalande, M. 1998. An imprinted antisense RNA overlaps UBE3A and a second maternally expressed transcript. Nature Genet. 19: 15–16.PubMedGoogle Scholar
  78. Rountree, M. and Selker, E.U. 1997. DNA methylation inhibits elongation but not initiation of transcription in Neurospora crassa. Genes Dev. 11: 2383–2393.PubMedGoogle Scholar
  79. Ryner, L.C. and Swain, A. 1995. Sex in the '90s. Cell 81: 483–493.PubMedGoogle Scholar
  80. Sänger, H.L. 1987. Viroid replication. In: T.O. Diener (Ed.) The Viroids, Plenum, New York, pp. 117–166.Google Scholar
  81. Schiebel, W., Pélissier, T., Riedel, L., Thalmeir, S., Schiebel, R., Kempe, D., Lottspeich, F., Sänger, H.L. and Wassenegger, M. 1998. Isolation of a RNA-directed RNA polymerase-specific cDNA clone from tomato leaf-tissue mRNA. Plant Cell 10: 2087–2101.PubMedGoogle Scholar
  82. Schmutte, C. and Jones, P.A. 1998. Involvement of DNA methylation in human carcinogenesis. Biol. Chem. 379: 377–388.PubMedGoogle Scholar
  83. Schuurs, T.A., Schaeffer, E.A.M. and Wessels, J.G.H. 1997. Homology-dependent silencing of the SC3 gene in Schizophyllum commune. Genetics 147: 589–596.PubMedGoogle Scholar
  84. Smilinich, N.J., Day, C.D., Fitzpatrick, G.V., Caldwell, G.M., Lossie, A.C., Cooper, P.R., Smallwood, A.C., Joyce, J.A., Schofield, P.N., Reik, W., Nicholls, R.D., Weksberg, R., Driscoll, D.J., Maher, E.R., Shows, T.B. and Higgins, M.J. 1999. A maternally methylated CpG island in KvLQT1 is associated with an antisense paternal transcript and loss of imprinting in Beckwith-Wiedemann syndrome. Proc. Natl. Acad. Sci. USA 96: 8064–8069.PubMedGoogle Scholar
  85. Smith, S.S. 1998. Stalling of DNA methyltransferase in chromosome stability and chromosome remodelling. Int. J. Mol. Med. 1: 147–156.PubMedGoogle Scholar
  86. Smith, H.A., Swaney, S.L., Parks, T.D., Wernsman, E.A. and Dougherty, W.G. 1994. Transgenic plant virus resistance mediated by untranslatable sense RNAs: expression, regulation, and fate of nonessential RNAs. Plant Cell 6: 1441–1453.CrossRefPubMedGoogle Scholar
  87. Stam, M., de Bruin, R., Kenter, S., van der Hoorn, R.A.L., van Blokland, R., Mol, J.N.M. and Kooter, J.M. 1997. Post-transcriptional silencing of chalcone synthase in Petunia by inverted transgene repeats. Plant J. 12: 63–82.Google Scholar
  88. Stam, M., Viterbo, A., Mol, J.N.M. and Kooter, J.M. 1998. Position-dependent methylation and transcriptional silencing of transgenes in inverted T-DNA repeats: implications for posttranscriptional silencing of homologous host genes in plants. Mol. Cell Biol. 18: 6165–6177.PubMedGoogle Scholar
  89. Tabara, H., Grishok, A. and Mello, C.C. 1998. RNAi in C. elegans: soaking in the genome sequence. Science 282: 430–431.PubMedGoogle Scholar
  90. Timmons, L. and Fire, A. 1998. Specific interference by ingested dsRNA. Nature 395: 854–854.PubMedGoogle Scholar
  91. Van Houdt, H., Ingelbrecht, I., Van Montagu, M. and Depicker, A. 1997. Post-transcriptional silencing of a neomycin phosphotransferase II transgene correlates with the accumulation of unproductive RNAs and with increased cytosine methylation of 3'-flanking regions. Plant J. 12: 379–392.Google Scholar
  92. Vaucheret, H. 1993. Identification of a general silencer for 19S and 35S promoters in a transgenic tobacco plant: 90 bp of homology in the promoter sequence are sufficient for trans-inactivation. C.R. Acad. Sci. Paris 316: 1471–1483.Google Scholar
  93. Vaucheret, H. 1994. Promoter-dependent trans-inactivation in transgenic tobacco plants: kinetic aspects of gene silencing and gene reactivation. C.R. Acad. Sci. Paris 317: 310–323.Google Scholar
  94. Vaucheret, H., Kronenberger, J., Lépingle, A., Vilaine, F., Boutin, J.P. and Caboche, M. 1992. Inhibition of tobacco nitrite reductase activity by expression of antisense RNA. Plant J. 2: 559–569.PubMedGoogle Scholar
  95. Voinnet, O., Vain, P., Angell, S. and Baulcombe, D.C. 1998. Systemic spread of sequence-specific transgene RNA degradation in plants is initiated by localized introduction of ectopic promoterless DNA. Cell 95: 177–187.PubMedGoogle Scholar
  96. Wade, P.A., Gegonne, A., Jones, P.L., Ballestar, E., Aubry, F. and Wolffe, A.P. 1999. Mi-2 complex couples DNA methylation to chromatin remodelling and histone deacetylation. Nature Genet. 23: 62–66.PubMedGoogle Scholar
  97. Wassenegger, M. and Pélissier, T. 1998. A model for RNA-mediated gene silencing in higher plants. Plant Mol. Biol. 37: 349–362.PubMedGoogle Scholar
  98. Wassenegger, M. and Pélissier, T. 1999. Signalling in gene silencing. Trends Plant Sci. 4: 207–209.PubMedGoogle Scholar
  99. Wassenegger, M., Heimes, S., Riedel, L. and Sänger, H.L. 1994. RNA-directed de novo methylation of genomic sequences in plants. Cell 76: 567–576.PubMedGoogle Scholar
  100. Waterhouse, P.M., Graham, M.W. and Wang, M.B. 1998. Virus resistance and gene silencing in plants can be induced by simultaneous expression of sense and antisense RNA. Proc. Natl. Acad. Sci. USA 95: 13959–13964.PubMedGoogle Scholar
  101. Wolffe, A.P. 1997. Sinful repression. Nature 387: 16–17.PubMedGoogle Scholar
  102. Wutz, A., Smrzka, O.W., Schweifer, N., Schellander, K., Wagner, E.F. and Barlow, D.P. 1997. Imprinted expression of the Igf2r gene depends on an intronic CpG island. Nature 389: 745–749.PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2000

Authors and Affiliations

  • Michael Wassenegger
    • 1
  1. 1.FhG Molekulare BiotechnologieMartinsriedGermany

Personalised recommendations