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.
Similar content being viewed by others
References
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.
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.
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.
Barlow, D.P., 1993. Methylation and imprinting: from host defense to gene regulation? Science 260: 309–310.
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.
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.
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.
Bestor, T. & B. Tycko, 1996. Creation of genomic methylation patterns. Nat. Genet. 12: 363–367.
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.
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.
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.
Birchler, J.A., M. Pal-Bhadra & U. Bhadra, 1999. Less from more: cosuppression of transposable elements. Natl. Genet. 21: 148–149.
Bird, A., 1997. Does DNA methylation control transposition of selfish elements in the germline? Trends Genet. 13: 469–470.
Bollman, J., R. Carpenter & E.S. Coen, 1991. Allelic interactions at the nivea locus of Antirrhinum. Plant Cell 3: 1327–1336.
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.
Britten, R.J., 1996 DNA sequence insertion and evolutionary variation in gene regulation. Proc. Natl. Acad. Sci. USA 93: 9374–9377.
Britten, R.J., 1997. Mobile elements inserted in the distant past have taken on important functions. Gene 205: 177–182.
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.
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.
Chadwick, D.J. & A.P. Wolffe, 1998. Novartis Foundation Symposium Vol 214, Epigenetics, Wiley, Chichester.
Cogoni C. & G. Macino, 1997. Conservation of transgene-induced post-transcriptional gene silencing in plants and fungi. Trends Plant Sci. 2: 438–443.
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.
Cogoni, C. & G. Macino, 1999. Gene silencing in Neurospora requires a protein homologous to RNA-dependent RNA polymerase. Nature 399: 166–169.
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.
Colot, V. & J.-L. Rossignol, 1999. Eukaryotic DNA methylation as an evolutionary device. BioEssays 21: 402–411.
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.
Coppin-Raynal, E., M. Picard & S. Arnaise, 1989. Transformation by integration in Podospora anserina. Mol. Gen. Genet. 219: 270–276.
Csink, A.K. & S. Henikoff, 1996. Genetic modification of heterochromatic association and nuclear organization in Drosophila. Nature 381: 529–531.
Cubas, P., C. Vincent & E. Coen, 1999. An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401: 157–161.
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.
Dorer, D.R. & S. Henikoff, 1994. Expansions of transgene repeats cause heterochromatin formation and gene silencing in Drosophila. Cell 77: 993–1002.
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.
Dupressoir, A. & T. Heidmann, 1996. Germ line-specific expression of intracisternal A-particle retrotransposons in transgenic mice. Mol. Cell Biol. 16: 4495–4503.
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.
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.
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.
Fire, A., 1999. RNA-triggered gene silencing. Trends Genet. 15: 358–363.
Gallardo, M.H., J.W. Bickham, R.L. Honeycutt, R.A. Ojeda & N. Köhler, 1999. Discovery of tetraploidy in a mammal. Nature 401: 341.
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.
Gonzalgo, M.L. & P.A. Jones, 1997. Mutagenic and epigenetic effects of DNA methylation. Mut. Res. 386: 107–118.
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.
Henikoff, S. & L. Comai, 1998. A DNA methyltransferase homolog with a chromodomain exists in multiple polymorphic forms in Arabidopsis. Genetics 149: 307–318.
Henikoff, S. & M.A. Matzke, 1997. Exploring and explaining epigenetic effects. Trends Genet. 13: 293–341.
Hiom, K., M. Melek & M. Gellert, 1998. DNA transposition by the RAG1 and RAG2 proteins: possible source of oncogenic translocations. Cell 94: 63–470.
Hollick, J.B., J.E. Dorweiler & V.L. Chandler, 1997. Paramutation & related allelic interactions. Trends Genet. 13: 293–341.
Horsthemke, B., B. Dittrich & K. Buiting, 1997. Imprinting mutations on human chromosome 15. Human Mutation 10: 329–337.
Jacobsen, S.E. & E.M. Meyerowitz, 1997. Hypermethylated SUPERMAN epigenetic alleles in Arabidopsis. Science 277: 1100–1103.
Jacobsen, S.E., 1999. Gene silencing: maintaining methylation patterns. Curr. Biol. 9: R617-R619.
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.
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.
Jensen, S., M.-P. Gassama & T. Heidmann, 1999. Taming of transposable elements by homology-dependent gene silencing. Nat. Genet. 21: 209–212.
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.
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.
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.
Kasschau, K.D. & J.C. Carrington, 1998. A counterdefensive strategy of plant viruses: suppression of post-transcriptional gene silencing. Cell 95: 461–470.
Kermicle, J.L., W.B. Eggleston & M. Alleman, 1995. Organization of paramutagenicity in R-stippled maize. Genetics 141: 361–372.
Kidwell, M. & D. Lisch, 1997. Transposable elements as sources of variation in animals and plants. Proc. Natl. Acad. Sci. USA 94: 7704–7711.
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.
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.
Lafontaine, D.L. & D. Tollervey, 1998. Birth of the snoRNPs: the evolution of the modification-guide snoRNAs. Trends Biochem. Sci. 23: 383–388.
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.
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.
Li, E., T.H. Bestor & R. Jaenisch, 1992. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69: 915–926.
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.
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.
Luff, B., L. Pawlowski & J. Bender, 1999. An inverted repeat triggers cytosine methylation of identical sequences in Arabidopsis. Mol. Cell 3: 505–511.
Lyon, M., 1998. X-chromosome inactivation: a repeat hypothesis. Cytogenet. Cell Genet. 80: 133–137.
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.
Martienssen, R., 1996. Epigenetic phenomena: paramutation and gene silencing in plants. Curr. Biol. 6: 810–813.
Masterson, J.S., 1994. Stomatal size in fossil plants: evidence for polyploidy in the majority of angiosperms. Science 264: 421–424.
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.
Matzke, A.J.M. & M.A. Matzke, 1998a. Position effects and epigenetic silencing of plant transgenes. Curr. Opin. Plant Biol. 1: 142–148.
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.
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.
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.
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.
McDonald, J.F., 1998. Transposable elements, gene silencing and macroevolution. Trends Ecol. Evol. 13: 94–95.
McDonald, J.F., 1993. Evolution and consequences of transposable elements. Curr. Opin. Genet. Devel. 3: 855–864.
McDonald, J.F., 1995. Transposable elements: possible catalysts of organismic evolution. Trends Ecol. Evol. 10: 123–126.
Melquist, S., B. Luff & J. Bender, 1999. Arabidopsis PAI gene arrangements, cytosine methylation and expression. Genetics 153: 401–413.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Ratcliff, F., B.D. Harrison & D.C. Baulcombe, 1997. A similarity between viral defense and gene silencing in plants. Science 276: 1558–1560.
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.
Richards, E., 1997. DNA methylation and plant development. Trends Genet. 13: 319–322.
Rossignol, J.-L. & G. Faugeron, 1994. Gene inactivation triggered by recognition between DNA repeats. Experientia 50: 307–317.
Russo, V.A., R. Martienssen & A. Riggs, 1996. Epigenetic Mechanisms of Gene Regulation, Cold Spring Harbor Press, New York.
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.
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.
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.
Selker, E.U., 1990. Premeiotic instability of repeated sequences in Neurospora. Annu. Rev. Genet. 24: 579–614.
Selker, E.U., 1997. Epigenetic phenomena in filamentous fungi: useful paradigms or repeat-induced confusion? Trends Genet. 13: 296–310.
Selker, E.U., 1999. Repeats that count. Cell 97: 157–160.
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.
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.
Singer, M., B. Marcotte & E. Selker, 1995. DNA methylation associated with repeat-induced point mutation in Neurospora crassa. Mol. Cell Biol. 15: 5586–5597.
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.
Smith, H., 1999. Interfering with viral infection: plants do it too. Plant Cell 11: 1191–1193.
Smith, C.M. & J.A. Steitz, 1997. Sno storm in the nucleolus: new roles for myriad small RNPs. Cell 89: 669–672.
Spring, J., 1997. Vertebrate evolution by interspecific hybridization-are we polyploid? FEBS Lett. 400: 2–8.
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.
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.
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.
Turker, M.S. & T.H. Bestor, 1997. Formation of methylation patterns in the mammalian genome. Mut. Res. 386: 119–130.
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.
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.
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.
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.
Voinnet, O. & D.C. Baulcombe, 1997. Systemic signaling in gene silencing. Nature 389: 553.
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.
Walker, E.L., 1998. Paramutation of the r1 locus of maize is associated with increased cytosine methylation. Genetics 148: 1973–1981.
Walsh, C.P. & T.H. Bestor, 1998. Transcription of IAP endogenous retroviruses is constrained by cytosine methylation. Nat. Genet. 20: 116–117.
Walsh, C.P. & T.H. Bestor, 1999. Cytosine methylation and mammalian development. Genes Devel. 13: 26–34.
Wassenegger, M. & T. Pélissier, 1998. A model for RNA-mediated gene silencing in higher plants. Plant Mol. Biol. 37: 349–362.
Wassenegger, M. & T. Pélissier, 1999. Signaling in gene silencing. Trends Plant Sci. 4: 207–209.
Wassenegger, M., S. Himes, L. Riedel & H. Sänger, 1994. RNA-directed de novo methylation of genomic sequences in plants. Cell 76: 567–576.
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.
Wessler, S., 1998. Transposable elements associated with normal plant genes. Physiologia Plantarum 103: 581–586.
Wolffe, A. & M.A. Matzke, 1999. Epigenetics: regulation through repression. Science, 286: 481–486.
Wu, C.-T. & J.R. Morris, 1999. Transvection and other homology effects. Curr. Opin. Genet. Dev. 9: 237–246.
Yoder, J. A., C. Walsh & T.H. Bestor, 1997. Cytosine methylation and the ecology of intragenomic parasites. Trends Genet. 13: 335–339.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Matzke, M., Mette, M., Aufsatz, W. et al. Host defenses to parasitic sequences and the evolution of epigenetic control mechanisms. Genetica 107, 271–287 (1999). https://doi.org/10.1023/A:1003921710672
Issue Date:
DOI: https://doi.org/10.1023/A:1003921710672