Genetica

, Volume 107, Issue 1–3, pp 271–287 | Cite as

Host defenses to parasitic sequences and the evolution of epigenetic control mechanisms

  • M.A. Matzke
  • M.F. Mette
  • W. Aufsatz
  • J. Jakowitsch
  • A.J.M. Matzke

Abstract

The analysis of transgene silencing effects in plants and other eukaryotic organisms has revealed novel mechanisms of epigenetic regulation that are based on recognition of nucleic acid sequence homology. These homology-dependent gene silencing phenomena are characterized by an inverse relationship between copy number of a particular sequence and expression levels. Depending on whether promoter regions or transcribed sequences are repeated, silencing occurs at the transcriptional or post-transcriptional level, respectively. Different silencing effects involving DNA–DNA or RNA–DNA associations in the nucleus, and RNA–RNA interactions in the cytoplasm appear to reflect distinct host defense responses to parasitic sequences, including transposable elements (TEs), viroids and RNA viruses. Natural epigenetic phenomena that resemble transgene silencing effects often involve endogenous genes comprising recognizable TE sequences or rearrangements generated by TEs and can thus be interpreted in terms of host defense systems. A genome defense that inactivates TEs by methylation might have been recruited during evolution to regulate the transcription of plant and vertebrate genes that contain remnants of TE insertions in promoter regions.

DNA methylation epigenetic silencing genome evolution polyploidy transgenic plants transposable elements viroids 

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References

  1. Agrawal, A., Q.M. Eastman & D.G. Schatz, 1998. Transposition mediated by RAG1 and RAG2 and its implications for the evolution of the immune system. Nature 394: 744–751.PubMedGoogle Scholar
  2. Anandalakshmi, R., G. Pruss, X. Ge, R. Marathe, A.C. Mallory, T.H. Smith & V.B. Vance, 1998. A viral suppressor of gene silencing in plants. Proc. Natl. Acad. Sci. USA 95: 13079–13084.PubMedGoogle Scholar
  3. Avramova, Z., A. Tikhonov, M. Chen & J.L. Bennetzen, 1998. Matrix attachment regions and structural colinearity in the genomes of two grass species. Nucl. Acids Res. 26: 761–777.PubMedGoogle Scholar
  4. Barlow, D.P., 1993. Methylation and imprinting: from host defense to gene regulation? Science 260: 309–310.PubMedGoogle Scholar
  5. Béclin, C., R. Berthomé, J.-C. Palauqui, M. Tepfer & H. Vaucheret, 1998. Infection of tobacco or Arabidopsis plants by CMV counteracts systemic post-transcriptional silencing of nonviral (trans)genes. Virology 252: 313–317.PubMedGoogle Scholar
  6. Bender, J. & G.R. Fink, 1995. Epigenetic control of an endogenous gene family is revealed by a novel blue fluorescent mutant of Arabidopsis. Cell 83: 725–734.PubMedGoogle Scholar
  7. Bennett, S.T., A.J. Wilson, L. Esposito, et al., 1997. Insulin VNTR allele-specific effect in type 1 diabetes depends on identity of untransmitted paternal allele. Nat. Genet. 17: 350–352.PubMedGoogle Scholar
  8. Bestor, T. & B. Tycko, 1996. Creation of genomic methylation patterns. Nat. Genet. 12: 363–367.PubMedGoogle Scholar
  9. Bestor, T., A. Laudano, R. Mattaliano & V. Ingram, 1988. Cloning and sequencing of a cDNA encoding DNA methyltransferase of mouse cells. J. Mol. Biol. 203: 971–983.PubMedGoogle Scholar
  10. Bestor, T.H., 1990. DNA methylation: evolution of a bacterial immune function into a regulator of gene expression and genome structure in higher eukaryotes. Phil. Trans. R. Soc. Lond. B 326: 179–187.Google Scholar
  11. Bestor, T.H., 1998. The host defense function of genomic methylation patterns. pp. 187–199 in Epigenetics edited by D.J. Chadwick and A.P. Wolffe, Novartis Foundation Symposium vol. 214, Wiley, Chichester.Google Scholar
  12. Birchler, J.A., M. Pal-Bhadra & U. Bhadra, 1999. Less from more: cosuppression of transposable elements. Natl. Genet. 21: 148–149.Google Scholar
  13. Bird, A., 1997. Does DNA methylation control transposition of selfish elements in the germline? Trends Genet. 13: 469–470.PubMedGoogle Scholar
  14. Bollman, J., R. Carpenter & E.S. Coen, 1991. Allelic interactions at the nivea locus of Antirrhinum. Plant Cell 3: 1327–1336.Google Scholar
  15. Brigneti, G., O. Voinnet, W.-X. Li, L.-H. Ji, S.-W. Ding & D.C. Baulcombe, 1998. Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana. EMBO J. 17: 6739–6746.PubMedGoogle Scholar
  16. Britten, R.J., 1996 DNA sequence insertion and evolutionary variation in gene regulation. Proc. Natl. Acad. Sci. USA 93: 9374–9377.PubMedGoogle Scholar
  17. Britten, R.J., 1997. Mobile elements inserted in the distant past have taken on important functions. Gene 205: 177–182.PubMedGoogle Scholar
  18. Casacuberta, E., J.M. Casacuberta, P. Puigdomènech & A. Monfort, 1998. Presence of miniature inverted-repeat transposable elements (MITES) in the genome of Arabidopsis thaliana: characterisation of the Emigrant family of elements. Plant J. 16: 79–85.PubMedGoogle Scholar
  19. Chaboissier, M.-C., A. Bucheton & D.J. Finnegan, 1998. Copy number control of a transposable element, the I factor, a LINE-like element in Drosophila. Proc. Natl. Acad. Sci. USA 95: 11781–11785.PubMedGoogle Scholar
  20. Chadwick, D.J. & A.P. Wolffe, 1998. Novartis Foundation Symposium Vol 214, Epigenetics, Wiley, Chichester.Google Scholar
  21. Cogoni C. & G. Macino, 1997. Conservation of transgene-induced post-transcriptional gene silencing in plants and fungi. Trends Plant Sci. 2: 438–443.Google Scholar
  22. Cogoni, C. & G. Macino, 1997. Isolation of quelling-defecive (qde) mutants imparied in posttranscriptional transgene-induced gene silencing in Neurospora crassa. Proc. Natl. Acad. Sci. USA 94: 10233–10238.PubMedGoogle Scholar
  23. Cogoni, C. & G. Macino, 1999. Gene silencing in Neurospora requires a protein homologous to RNA-dependent RNA polymerase. Nature 399: 166–169.PubMedGoogle Scholar
  24. Cogoni, C., J. Irelan, M. Schumacher, T. Schmidhauser, E. Selker & G. Macino, 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
  25. Colot, V. & J.-L. Rossignol, 1999. Eukaryotic DNA methylation as an evolutionary device. BioEssays 21: 402–411.PubMedGoogle Scholar
  26. Colot, V., L. Maloisel & J.-L. Rossignol, 1997. Interchromosomal transfer of epigenetic states in Ascobolus: transfer of DNA methylation is mechanistically related to homologous recombination. Cell 86: 855–864.Google Scholar
  27. Coppin-Raynal, E., M. Picard & S. Arnaise, 1989. Transformation by integration in Podospora anserina. Mol. Gen. Genet. 219: 270–276.PubMedGoogle Scholar
  28. Csink, A.K. & S. Henikoff, 1996. Genetic modification of heterochromatic association and nuclear organization in Drosophila. Nature 381: 529–531.PubMedGoogle Scholar
  29. Cubas, P., C. Vincent & E. Coen, 1999. An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401: 157–161.PubMedGoogle Scholar
  30. DeBerardinis, R.J., J.L. Goodier, E.M. Ostertag & H.H. Kazazian, 1998. Rapid amplification of a retrotransposon subfamily is evolving the mouse genome. Nat. Genet. 20: 288–290.PubMedGoogle Scholar
  31. Dorer, D.R. & S. Henikoff, 1994. Expansions of transgene repeats cause heterochromatin formation and gene silencing in Drosophila. Cell 77: 993–1002.PubMedGoogle Scholar
  32. Dorer, D.R. & S. Henikoff, 1997. Transgene repeat arrays interact with distant heterochromatin and cause silencing in cis and in trans. Genetics 147: 1181–1190.PubMedGoogle Scholar
  33. Dupressoir, A. & T. Heidmann, 1996. Germ line-specific expression of intracisternal A-particle retrotransposons in transgenic mice. Mol. Cell Biol. 16: 4495–4503.PubMedGoogle Scholar
  34. Elmayan, T., S. Balzergue, F. Béon, V. Bourdon, J. Daubremet, Y. Guénet, P. Mourrain, J.-C. Palauqui, S. Vernhettes, T. Vialle, K. Wostrikoff & H. Vaucheret, 1998. Arabidopsis mutants impaired in cosuppression. Plant Cell 10: 1747–1757.PubMedGoogle Scholar
  35. English, J.J., E. Mueller & D.C. Baulcombe, 1996. Suppression of virus accumulation in transgenic plants exhibiting silencing of nuclear genes. Plant Cell 8: 179–188.PubMedGoogle Scholar
  36. Finnegan, E.J., R.K. Genger, W.J. Peacock & E.S Dennis, 1998. DNA methylation in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49: 223–248.PubMedGoogle Scholar
  37. Fire, A., 1999. RNA-triggered gene silencing. Trends Genet. 15: 358–363.PubMedGoogle Scholar
  38. Gallardo, M.H., J.W. Bickham, R.L. Honeycutt, R.A. Ojeda & N. Köhler, 1999. Discovery of tetraploidy in a mammal. Nature 401: 341.PubMedGoogle Scholar
  39. Goodwin, J., K. Chapman, S. Swaney, T.D. Parks, E.A. Wernsman & W.G. Dougherty, 1996. Genetic and biochemical dissection of transgenic RNA-mediated virus resistance. Plant Cell 8: 95–105.PubMedGoogle Scholar
  40. Gonzalgo, M.L. & P.A. Jones, 1997. Mutagenic and epigenetic effects of DNA methylation. Mut. Res. 386: 107–118.Google Scholar
  41. Hendrich, B., U. Hardeland, H.-H. Ng, J. Jiricny & A. Bird, 1999. The thymine glycosylase MBD4 can bind to the product of deamination at methylated CpG sites. Nature 401: 301–304.PubMedGoogle Scholar
  42. Henikoff, S. & L. Comai, 1998. A DNA methyltransferase homolog with a chromodomain exists in multiple polymorphic forms in Arabidopsis. Genetics 149: 307–318.PubMedGoogle Scholar
  43. Henikoff, S. & M.A. Matzke, 1997. Exploring and explaining epigenetic effects. Trends Genet. 13: 293–341.PubMedGoogle Scholar
  44. Hiom, K., M. Melek & M. Gellert, 1998. DNA transposition by the RAG1 and RAG2 proteins: possible source of oncogenic translocations. Cell 94: 63–470.Google Scholar
  45. Hollick, J.B., J.E. Dorweiler & V.L. Chandler, 1997. Paramutation & related allelic interactions. Trends Genet. 13: 293–341.Google Scholar
  46. Horsthemke, B., B. Dittrich & K. Buiting, 1997. Imprinting mutations on human chromosome 15. Human Mutation 10: 329–337.PubMedGoogle Scholar
  47. Jacobsen, S.E. & E.M. Meyerowitz, 1997. Hypermethylated SUPERMAN epigenetic alleles in Arabidopsis. Science 277: 1100–1103.PubMedGoogle Scholar
  48. Jacobsen, S.E., 1999. Gene silencing: maintaining methylation patterns. Curr. Biol. 9: R617-R619.PubMedGoogle Scholar
  49. Jakowitsch, J., I. Papp, E.A. Moscone, J. van der Winden, M. Matzke & A.J.M. Matzke, 1999. Molecular and cytogenetic characterization of a transgene locus that induces silencing and methylation of homologous promoters in trans. Plant J. 17: 131–140.PubMedGoogle Scholar
  50. Jeddeloh, J.A., T.L. Stokes & E.J. Richards, 1999. Maintenance of genomic methylation requires a SWI2/SNF2-like protein. Nat. Genet. 22: 94–96.PubMedGoogle Scholar
  51. Jensen, S., M.-P. Gassama & T. Heidmann, 1999. Taming of transposable elements by homology-dependent gene silencing. Nat. Genet. 21: 209–212.PubMedGoogle Scholar
  52. Jones, A.L., C.L. Thomas & A.J. Maule, 1998. De novo methylation and cosuppression induced by a cytoplasmically replicating plant RNA virus. EMBO J. 17: 6385–6393.PubMedGoogle Scholar
  53. Jones, P.L., G. Veenstra, P.A. Wade, D. Vermaak, S.U. Kass, N. Landsberger, J. Strouboulis & A.P. Wolffe, 1998. Methylated DNA & MeCP2 recruit histone deacetylase to repress transcription. Nat. Genet. 19: 187–191.PubMedGoogle Scholar
  54. Jorgensen, R.A., R.G. Atkinson, R.L.S. Forster & W.J. Lucas, 1998. An RNA-based information superhighway in plants. Science 279: 1486–1487.PubMedGoogle Scholar
  55. Kasschau, K.D. & J.C. Carrington, 1998. A counterdefensive strategy of plant viruses: suppression of post-transcriptional gene silencing. Cell 95: 461–470.PubMedGoogle Scholar
  56. Kermicle, J.L., W.B. Eggleston & M. Alleman, 1995. Organization of paramutagenicity in R-stippled maize. Genetics 141: 361–372.PubMedGoogle Scholar
  57. Kidwell, M. & D. Lisch, 1997. Transposable elements as sources of variation in animals and plants. Proc. Natl. Acad. Sci. USA 94: 7704–7711.PubMedGoogle Scholar
  58. Kiefer, M.C., R.A. Owens & T.O. Diener, 1983. Structural similarities between viroids and transposable genetic elements. Proc. Natl. Acad. Sci. USA 80: 6234–6238.PubMedGoogle Scholar
  59. Kooter, J., M.A. Matzke & P. Meyer, 1999. Listening to the silent genes: transgene silencing, gene regulation and pathogen control. Trends Plant Sci. 4: 340–347.PubMedGoogle Scholar
  60. Lafontaine, D.L. & D. Tollervey, 1998. Birth of the snoRNPs: the evolution of the modification-guide snoRNAs. Trends Biochem. Sci. 23: 383–388.PubMedGoogle Scholar
  61. Lee, J.T., L.S. Davidow & D. Warshawsky, 1999. Tsix, a gene antisense to Xist at the X-inactivation center. Nat. Genet. 21: 400–404.PubMedGoogle Scholar
  62. Levis, R., R. Ganesan, K. Houtchens, L.A. Tolar & F.-M. Sheen, 1993. Transposons in place of telomeric repeats at a Drosophila telomere. Cell 75: 1083–1093.PubMedGoogle Scholar
  63. Li, E., T.H. Bestor & R. Jaenisch, 1992. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69: 915–926.PubMedGoogle Scholar
  64. Li, H.-W., A.P. Lucy, H.-S. Guo, W.-X. Li, L.-H. Ji, S.-M. Wong & S.-W. Ding, 1999. Strong host resistance targeted against a viral suppressor of the plant gene silencing defence mechanisms. EMBO J. 18: 2683–2691.PubMedGoogle Scholar
  65. Lindbo, J.A., L. Silva-Rosales, W.M. Proebsting & W.G. Dougherty, 1993. Induction of a highly specific antiviral state in transgenic plants: implications for regulation of gene expression and virus resistance. Plant Cell 5: 1749–1759.PubMedGoogle Scholar
  66. Luff, B., L. Pawlowski & J. Bender, 1999. An inverted repeat triggers cytosine methylation of identical sequences in Arabidopsis. Mol. Cell 3: 505–511.PubMedGoogle Scholar
  67. Lyon, M., 1998. X-chromosome inactivation: a repeat hypothesis. Cytogenet. Cell Genet. 80: 133–137.PubMedGoogle Scholar
  68. Malagnac, F., F. Wendel, C. Goyon, G. Faugeron, D. Zickler, J.-L. Rossignol, M. Noyer-Weldner, T. Trautner & J. Walter, 1997. A gene essential for de novo methylation and development in Ascobolus reveals a novel type of eukaryotic DNA methyltransferase structure. Cell 91: 1–20.Google Scholar
  69. Martienssen, R., 1996. Epigenetic phenomena: paramutation and gene silencing in plants. Curr. Biol. 6: 810–813.PubMedGoogle Scholar
  70. Masterson, J.S., 1994. Stomatal size in fossil plants: evidence for polyploidy in the majority of angiosperms. Science 264: 421–424.Google Scholar
  71. Matzke, A.J.M., F. Neuhuber, Y.-D. Park, P. Ambros & M.A. Matzke, 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
  72. Matzke, A.J.M. & M.A. Matzke, 1998a. Position effects and epigenetic silencing of plant transgenes. Curr. Opin. Plant Biol. 1: 142–148.PubMedGoogle Scholar
  73. Matzke, M.A. & A.J.M. Matzke, 1998b. Epigenetic silencing of plant transgenes as a consequence of distinct cellular defense responses. Cell Mol. Life Sci. 54: 94–103.PubMedGoogle Scholar
  74. Matzke, M.A. & A.J.M. Matzke, 1998c. Gene silencing in plants: relevance for genome evolution and the acquisition of genomic methylation patterns. pp.168–186 in Epigenetics edited by D.J. Chadwick and A.P. Wolffe, Novartis Foundation Symposium vol 214, Wiley Chichester.Google Scholar
  75. Matzke, M.A., A.J.M. Matzke & W. Eggleston, 1996. Transgene silencing and paramutation: a common response to invasive DNA? Trends Plant Sci. 1: 382–388.Google Scholar
  76. Matzke, M.A., M.P. Primig, J. Trnovsky & A.J.M. Matzke, 1989. Reversible methylation and inactivation of marker genes in sequentially transformed tobacco plants. EMBO J. 8: 643–649.PubMedGoogle Scholar
  77. McDonald, J.F., 1998. Transposable elements, gene silencing and macroevolution. Trends Ecol. Evol. 13: 94–95.Google Scholar
  78. McDonald, J.F., 1993. Evolution and consequences of transposable elements. Curr. Opin. Genet. Devel. 3: 855–864.Google Scholar
  79. McDonald, J.F., 1995. Transposable elements: possible catalysts of organismic evolution. Trends Ecol. Evol. 10: 123–126.Google Scholar
  80. Melquist, S., B. Luff & J. Bender, 1999. Arabidopsis PAI gene arrangements, cytosine methylation and expression. Genetics 153: 401–413.PubMedGoogle Scholar
  81. Mette, M.F., J. van der Winden, M.A. Matzke & A.J.M. Matzke, 1999. Production of aberrant promoter transcripts contributes to methylation and silencing of unlinked homologous promoters in trans. EMBO J. 18: 241–248.PubMedGoogle Scholar
  82. Meyer, P., I. Heidmann & I. Niedenhof, 1993. Differences in DNA methylation are associated with a paramutation phenomenon in transgenic petunia. Plant J. 4: 89–100.PubMedGoogle Scholar
  83. Mittelsten Scheid, O., K. Afsar & J. Paszkowski, 1998. Release of epigenetic silencing by trans-acting mutations in Arabidopsis. Proc. Natl. Acad. Sci. USA 95: 632–637.PubMedGoogle Scholar
  84. Nan, X., H.-H. Ng, C.A. Johnson, C.D. Laherty, B.M. Turner, R.N. Eisenman & A. Bird, 1998. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393: 386–389.PubMedGoogle Scholar
  85. Napoli, C., C. Lemieux & R. Jorgensen, 1990. Introduction of a chimeric chalcone synthase gene into petunia results in reversible cosuppression of homologous genes in trans. Plant Cell 2: 279–289.PubMedGoogle Scholar
  86. Ng, H.-H., Y. Zhang, B. Hendrich, C.A. Johnson, B.M. Turner, H. Erdjument-Bromage, P. Tempst, D. Reinberg & A. Bird, 1999. MBD2 is a transcriptional repressor belonging to the MeCP1 histone deacetylase complex. Nat. Genet. 23: 58–61.PubMedGoogle Scholar
  87. O'Neill, R.J., M.J. O'Neill & J.A. Graves, 1998. Undermethylation associated with retroelement activation and chromosome remodeling in an interspecific mammalian hybrid. Nature 393: 68–72.PubMedGoogle Scholar
  88. Palauqui, J.-C., T. Elmayan, J.-M. Pollien & H. Vaucheret, 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
  89. Pal-Bhadra, M., U. Bhadra & J.A. Birchler, 1997. Cosuppression in Drosophila: gene silencing of Alcohol dehydrogenase by white-Adh transgenes is Polycomb dependent. Cell 90: 479–490.PubMedGoogle Scholar
  90. Park, Y.-D., I. Papp, E.A. Moscone, V.A. Iglesias, H. Vaucheret, A.J.M. Matzke & M.A. Matzke, 1996. Gene silencing mediated by promoter homology occurs at the level transcription and results in meiotically heritable alterations in methylation and gene activity. Plant J. 9: 183–194.PubMedGoogle Scholar
  91. Pélissier, T., S. Tutois, J.M. Deragon, S. Tourmente, S. Genestier & G. Picard, 1995. Athila, a new retroelement from Arabidopsis thaliana. Plant Mol. Biol. 29: 441–452.PubMedGoogle Scholar
  92. Ratcliff, F., B.D. Harrison & D.C. Baulcombe, 1997. A similarity between viral defense and gene silencing in plants. Science 276: 1558–1560.Google Scholar
  93. Regev, A., M. Lamb & E. Jablonka, 1998. The role of DNA methylation in invertebrates: developmental regulation or genome defense? Mol. Biol. Evol. 15: 880–891.Google Scholar
  94. Richards, E., 1997. DNA methylation and plant development. Trends Genet. 13: 319–322.PubMedGoogle Scholar
  95. Rossignol, J.-L. & G. Faugeron, 1994. Gene inactivation triggered by recognition between DNA repeats. Experientia 50: 307–317.PubMedGoogle Scholar
  96. Russo, V.A., R. Martienssen & A. Riggs, 1996. Epigenetic Mechanisms of Gene Regulation, Cold Spring Harbor Press, New York.Google Scholar
  97. SanMiguel, P., B.S. Gaut, A. Tikhonov, Y. Nakajima & J.L. Bennetzen, 1998. The paleontology of intergenic retrotransposons of maize. Nat. Genet. 20: 43–45.PubMedGoogle Scholar
  98. SanMiguel, P., A. Tikhonov, Y. Jin, N. Motchoulskaia, D. Zakharov, A. Melake-Berhan, P.S. Springer, K.J. Edwards, M. Lee, Z. Avramova & J.L. Bennetzen, 1996. Nested retrotransposons in the intergenic regions of the maize genome. Science 274: 765–768.PubMedGoogle Scholar
  99. Schiebel, W., T. Pélissier, L. Riedel, S. Thalmeir, R. Schiebel, D. Kempe, F. Lottspeich, H. Sänger & M. Wassenegger, 1998. Isolation of an RNA-directed RNA polymerase-specific cDNA clone from tomato. Plant Cell 10: 2087–2101.PubMedGoogle Scholar
  100. Selker, E.U., 1990. Premeiotic instability of repeated sequences in Neurospora. Annu. Rev. Genet. 24: 579–614.PubMedGoogle Scholar
  101. Selker, E.U., 1997. Epigenetic phenomena in filamentous fungi: useful paradigms or repeat-induced confusion? Trends Genet. 13: 296–310.PubMedGoogle Scholar
  102. Selker, E.U., 1999. Repeats that count. Cell 97: 157–160.PubMedGoogle Scholar
  103. Sheen, F.-M. & R.W. Levis, 1994. Transposition of the LINE-like retrotransposon TART to Drosophila chromosome termini. Proc. Natl. Acad. Sci. USA 91: 12510–12514.PubMedGoogle Scholar
  104. Simmen, M.W., S. Leitgeb, J. Charlton, S.J.M. Jones, B.R. Harris, V.H. Clark & A. Bird, 1999. Nonmethylated transposable elements and methylated genes in a chordate genome. Science 283: 1164–1167.PubMedGoogle Scholar
  105. Singer, M., B. Marcotte & E. Selker, 1995. DNA methylation associated with repeat-induced point mutation in Neurospora crassa. Mol. Cell Biol. 15: 5586–5597.PubMedGoogle Scholar
  106. Smith, C.J.S., C.F. Watson, C.R. Bird, J. Ray, W. Schuch & D. Grierson, 1990. Expression of a truncated tomato polygalacturonase gene inhibits expression of the endogenous gene in transgenic plants. Mol. Gen. Genet. 224: 447–481.Google Scholar
  107. Smith, H., 1999. Interfering with viral infection: plants do it too. Plant Cell 11: 1191–1193.PubMedGoogle Scholar
  108. Smith, C.M. & J.A. Steitz, 1997. Sno storm in the nucleolus: new roles for myriad small RNPs. Cell 89: 669–672.PubMedGoogle Scholar
  109. Spring, J., 1997. Vertebrate evolution by interspecific hybridization-are we polyploid? FEBS Lett. 400: 2–8.PubMedGoogle Scholar
  110. Stam, M., A. Viterbo, J.N.M. Mol & J.M. Kooter, 1998. Positiondependent 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
  111. Stinard, P.S., D.S. Robertson & P.S. Schnable, 1993. Genetic isolation, cloning, and analysis of a Mutator-induced, dominant antimorph of the maize amylose extender 1 locus. Plant Cell 5: 1555–1566.PubMedGoogle Scholar
  112. Todd, J.J. & L.O. Vodkin, 1996. Duplications that suppress and deletions that restore expression from a chalcone synthase multigene family. Plant Cell 8: 687–699.PubMedGoogle Scholar
  113. Turker, M.S. & T.H. Bestor, 1997. Formation of methylation patterns in the mammalian genome. Mut. Res. 386: 119–130.Google Scholar
  114. van Blokland, R., N. van der Geest, J.N.M. Mol & J.M. Kooter, 1994. Transgene-mediated suppression of chalcone synthase expression in Petunia hybrida results from an increase in RNA turnover. Plant J. 6: 861–877.Google Scholar
  115. van der Krol, A.R., L.A. Mur, M. Beld, J.N.M. Mol & A.R. Stuitje, 1990. Flavonoid genes in petunia: addition of a limited number of gene copies may lead to a suppression of gene expression. Plant Cell 2: 291–299.PubMedGoogle Scholar
  116. Van Houdt, H., I. Ingelbrecht, M. Van Montagu & A. Depicker, 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
  117. Vaucheret, H., 1993. Identification of a general silencer for 19S and 35S promoters in a transgenic tobacco plants: 90 bp of homology in the promoter region are sufficient for trans-inactivation. C.R. Acad. Sci. Paris 316: 1471–1483.Google Scholar
  118. Voinnet, O. & D.C. Baulcombe, 1997. Systemic signaling in gene silencing. Nature 389: 553.PubMedGoogle Scholar
  119. Wade, P.A., A. Gegonne, P.L. Jones, E. Ballestar, F. Aubry & A.P. Wolffe, 1999. Mi-2 complex couples DNA methylation to chromatin remodeling and histone deacetylation. Nat. Genet. 23: 62–66.PubMedGoogle Scholar
  120. Walker, E.L., 1998. Paramutation of the r1 locus of maize is associated with increased cytosine methylation. Genetics 148: 1973–1981.PubMedGoogle Scholar
  121. Walsh, C.P. & T.H. Bestor, 1998. Transcription of IAP endogenous retroviruses is constrained by cytosine methylation. Nat. Genet. 20: 116–117.PubMedGoogle Scholar
  122. Walsh, C.P. & T.H. Bestor, 1999. Cytosine methylation and mammalian development. Genes Devel. 13: 26–34.PubMedGoogle Scholar
  123. Wassenegger, M. & T. Pélissier, 1998. A model for RNA-mediated gene silencing in higher plants. Plant Mol. Biol. 37: 349–362.PubMedGoogle Scholar
  124. Wassenegger, M. & T. Pélissier, 1999. Signaling in gene silencing. Trends Plant Sci. 4: 207–209.PubMedGoogle Scholar
  125. Wassenegger, M., S. Himes, L. Riedel & H. Sänger, 1994. RNA-directed de novo methylation of genomic sequences in plants. Cell 76: 567–576.PubMedGoogle Scholar
  126. Waterhouse, P.M., H.W. Graham & M.B. Wang, 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
  127. Wessler, S., 1998. Transposable elements associated with normal plant genes. Physiologia Plantarum 103: 581–586.Google Scholar
  128. Wolffe, A. & M.A. Matzke, 1999. Epigenetics: regulation through repression. Science, 286: 481–486.PubMedGoogle Scholar
  129. Wu, C.-T. & J.R. Morris, 1999. Transvection and other homology effects. Curr. Opin. Genet. Dev. 9: 237–246.PubMedGoogle Scholar
  130. Yoder, J. A., C. Walsh & T.H. Bestor, 1997. Cytosine methylation and the ecology of intragenomic parasites. Trends Genet. 13: 335–339.PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 1999

Authors and Affiliations

  • M.A. Matzke
    • 1
  • M.F. Mette
    • 1
  • W. Aufsatz
    • 1
  • J. Jakowitsch
    • 1
  • A.J.M. Matzke
    • 1
  1. 1.Institute of Molecular BiologyAustrian Academy of SciencesSalzburgAustria, (E-mail

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