Skip to main content
Log in

Role of inverted DNA repeats in transcriptional and post-transcriptional gene silencing

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Transgenes and endogenous genes are sensitive to silencing, in particular when the genes are tandemly repeated. Their expression can be transcriptionally or post-transcriptionally repressed, or both. It is remarkable that very often, two or more genes or parts of the genes are arranged as inverted repeats (IR). Many of such IRs are dominant silencing loci. They can repress the expression of homologous genes elsewhere in the genome in trans which is usually associated with an increase in the level of DNA methylation. Trans-silencing has been explained by DNA-DNA pairing between a repetitive silencing locus and a homologous target locus. However, there is accumulating evidence that the trans effect might be mediated by dsRNA transcribed from the IR (trans)genes. Besides dsRNA-directed DNA methylation, dsRNA in plants as well as in other systems also induces the degradation of homologous RNAs and silence genes post-transcriptionally. These findings indicate that several features associated with gene silencing can be attributed to the activities of dsRNA, which would explain why inverted transgene repeats are such efficient silencing loci.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Akgün, E., Zahn, J., Baumes, S., Brown, G., Liang, F., Romanienko, P.J., Lewis, S. and Jasin, M. 1997. Palindrome resolution and recombination in the mammalian germ line. Mol. Cell. Biol. 17: 5559–5570.

    PubMed  Google Scholar 

  • Angell, S.M. and Baulcombe, D.C. 1997. Consistent gene silencing in transgenic plants expressing a replicating potato virus X RNA. EMBO J. 16: 3675–3684.

    PubMed  Google Scholar 

  • Assaad, F.F., Tucker, K.L. and Signer, E.R. 1993. Epigenetic repeatinduced gene silencing (RIGS) in Arabidopsis. Plant Mol. Biol. 22: 1067–1085.

    PubMed  Google Scholar 

  • Baulcombe, D.C. and English, J.J. 1996. Ectopic pairing of homologous DNA and post-transcriptional silencing in transgenic plants. Curr. Opin. Biotechnol. 7: 173–180.

    Google Scholar 

  • Bender, J. 1998. Cytosine methylation of repeated sequences in eukaryotes: the role of DNA pairing. Trends Biochem. Sci. 23: 252–256.

    PubMed  Google Scholar 

  • Bender, J. and Fink, G.R. 1995. Epigenetic control of an endogenous gene family is revealed by a novel blue fluorescent mutant of Arabidopsis. Cell 83: 725–734.

    PubMed  Google Scholar 

  • Bestor, T.H. 1987. Supercoiling-dependent sequence specificity of mammalian DNA methyltransferase. Nucl. Acids Res. 15: 3835–3843.

    PubMed  Google Scholar 

  • Bestor, T.H. and Coxon, A. 1993. Cytosine methylation: the pros and cons of DNA methylation. Curr. Biol. 3: 384–386.

    PubMed  Google Scholar 

  • Bi, X. and Liu, L.F. 1996. DNA rearrangement mediated by inverted repeats. Proc. Natl. Acad. Sci. USA 93: 819–823.

    PubMed  Google Scholar 

  • Bird, A.P. and Wolffe, A.P. 1999. Methylation-induced repression: belts, braces and chromatin. Cell 99: 451–454.

    PubMed  Google Scholar 

  • Blaho, A.J., Larson, J.E., McLean, M.J. and Wells, R.D. 1988. Multiple DNA secondary structures in perfect inverted repeat inserts in plasmids. J. Biol. Chem. 263: 14446–14455.

    PubMed  Google Scholar 

  • Bollmann, J., Carpenter, R. and Coen, E.S. 1991. Allelic interactions at the nivea locus of Antirrhinum. Plant Cell 3: 1327–1336.

    Article  PubMed  Google Scholar 

  • Christou, P. 1992. Genetic transformation of crop plants using microprojectile bombardment. Plant J. 2: 275–281.

    Google Scholar 

  • Cluster, P., O'Dell, M., Metzlaff, M. and Flavell, R.B. 1996. Details of T-DNA structural organization from a transgenic Petunia population exhibiting co-suppression. Plant Mol. Biol. 32: 1197–1203.

    PubMed  Google Scholar 

  • Coen, E.S. and Carpenter, R. 1988. A semi-dominant allele, niv-525, acts in trans to inhibit the expression of its wild-type homologue in Antirrhinum majus. EMBO J. 7: 877–883.

    PubMed  Google Scholar 

  • Cogoni, C. and Macino, G. 1999. Homology-dependent gene silencing in plants and fungi: a number of variations on the same theme. Curr. Opin. Microbiol. 2: 657–662.

    PubMed  Google Scholar 

  • Collick, A., Drew, J., Penberth, J., Bois, P., Luckett, J., Scaerou, F., Jeffreys, A. and Reik, W. 1996. Instability of long inverted repeats within mouse transgenes. EMBO J. 15: 1163–1171.

    PubMed  Google Scholar 

  • Collins, J. 1980. Instability of palindromic DNA in Escherichia coli. Cold Spring Harbor Symp. Quant. Biol. 45: 409–416.

    Google Scholar 

  • Collins, J., Volkaert, G. and Nevers, P. 1982. Precise and nearlyprecise excision of the symmetrical inverted repeats of Tn5; common features of recA-independent deletion events in Escherichia coli. Gene 19: 139–146.

    PubMed  Google Scholar 

  • Colot, V., Maloisel, L. and Rossignol, J.L. 1996. Interchromosomal transfer of epigenetic states in Ascobolus: transfer of DNA methylation is mechanistically related to homologous recombination. Cell 86: 855–864.

    PubMed  Google Scholar 

  • DasGupta, U., Weston-Hafer, K. and Berg, D.E. 1987. Local DNA sequence control of deletion formation in Escherichia coli plasmid pBR322. Genetics 115: 41–49.

    PubMed  Google Scholar 

  • Dehio, C. and Schell, J. 1994. Identification of plant genetic loci involved in a posttranscriptional mechanism for meiotically reversible transgene silencing. Proc. Natl. Acad. Sci. USA 91: 5538–5542.

    PubMed  Google Scholar 

  • De Neve, M., De Buck, S., Jacobs, A., Van Montagu, M. and Depicker, A. 1997. T-DNA integration patterns in cotransformed plant cells suggest that T-DNA repeats originate from co-integration of separate T-DNAs. Plant J. 11: 15–29.

    PubMed  Google Scholar 

  • Depicker, A., Ingelbrecht, I., Van Houdt, H., De Loose, M. and Van Montagu, M. 1996. Post-transcriptional reporter transgene silencing in transgenic tobacco. In: D. Grierson, G.W. Lycett and G.A. Tucker GA (Eds.) Mechanisms and Applications of Gene Silencing, Nottingham University Press, Nottingham, UK, pp. 71–84.

    Google Scholar 

  • Dorer, D.R. 1997. Do transgene arrays form heterochromatin in vertebrates? Transgen. Res. 6: 3–10.

    Google Scholar 

  • Dorer, D.R. and Henikoff, S. 1994. Expansions of transgene repeats cause heterochromatin formation and gene silencing in Drosophila. Cell 77: 993–1002.

    Google Scholar 

  • Dorer, D.R. and Henikoff, S. 1997. Transgene repeat arrays interact with distant heterochromatin and cause silencing in cis and trans. Genetics 147: 1181–1190.

    PubMed  Google Scholar 

  • Ehrlich, S.D. 1989. Illegitimate recombination in bacteria. In: D.E. Berg and M.M. Howe (Eds.)Mobile DNA, American Society for Microbiology, Washington, D.C., pp. 799–832.

    Google Scholar 

  • Elmayan, T. and Vaucheret, H. 1996. A strongly-expressed 35Sdriven transgene undergoes post-transcriptional silencing in all tobacco transformants irrespective of the copy number. Plant J. 9: 787–797.

    Google Scholar 

  • English, J.J., Mueller, E. and Baulcombe, D.C. 1996. Suppression of virus accumulation in transgenic plants exhibiting silencing of nuclear genes. Plant Cell 8: 179–188.

    Article  PubMed  Google Scholar 

  • English, J.J., Davenport, G.F., Elmayan, T., Vaucheret, H. and Baulcombe, D.C. 1997. Requirement of sense transcription for homology-dependent virus resistance and trans-inactivation. Plant J. 12: 597–603.

    Google Scholar 

  • Faugeron. G., Rhounim, L. and Rossignol, J.-L. 1990. How does the cell count the number of ectopic copies of a gene in the premeiotic inactivation process acting in Ascobolus immersus. Genetics 135: 357–366.

    Google Scholar 

  • Fire, A. 1999. RNA-triggered gene silencing. Trends Genet. 15: 358–363.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Garrick, D., Fiering, S., Martin, D.I.K. and Whitelaw, E. 1998. Repeat-induced gene silencing in mammals. Nature Genet. 18: 56–59.

    PubMed  Google Scholar 

  • Goodwin, J., Chapman, K., Swaney, S., Parks, T.D., Wernsman, E.A. and Dougherty, W.G. 1996. Genetic and biochemical dissection of transgenic RNA-mediated virus resistance. Plant Cell 8: 95–105.

    PubMed  Google Scholar 

  • Gordenin, D.A., Lobachev, K.S., Degtyareva, N.P., Malkova, A.L., Perkins, E. and Resnick, M.A. 1993. Inverted DNA repeats: a source of eukaryotic genomic instability. Mol. Cell. Biol. 13: 5315–5322.

    PubMed  Google Scholar 

  • Goyon, C., Nogueira, T.I.V. and Faugeron, G. 1994. Perpetuation of cytosine methylation in Ascobolus immersus implies a novel type of maintenance methylase. J. Mol. Biol. 240: 42–51.

    PubMed  Google Scholar 

  • Hamilton, A.J., Brown, S., Han, Y.H., Ishizuka, M., Lowe, A., Solis, A.G.A. and Grierson, D. 1998. A transgene with repeated DNA causes high-frequency, post-transcriptional suppression of ACCoxidase gene expression in tomato. Plant J. 15: 737–746.

    Google Scholar 

  • Hanke, J.H., Hambor, J.E. and Kavathas, P. 1995. Repetitive Alu elements form a cruciform structure that regulates the function of the human CD8a T cell-specific enhancer. J. Mol. Biol. 246: 63–73.

    PubMed  Google Scholar 

  • Henikoff, S. and Comai, L. 1998. Trans-sensing effects: the ups and downs of being together. Cell 93: 329–332.

    PubMed  Google Scholar 

  • Hobbs, S.L.A., Kpodar, P. and Delong, C.M.O. 1990. The effect of T-DNA copy number, position and methylation on reporter gene expression in tobacco transformants. Plant Mol. Biol. 15: 851–864.

    PubMed  Google Scholar 

  • Hobbs, S.L.A., Warkentin, T.D. and Delong, C.M.O. 1993. Transgene copy number can be positively or negatively associated with transgene expression. Plant Mol. Biol. 21: 17–26.

    PubMed  Google Scholar 

  • Hollick, J.B., Dorweiler, J.E. and Chandler, V.L. 1997. Paramutation and related allelic interactions. Trends Genet. 13: 302–308.

    PubMed  Google Scholar 

  • Ingelbrecht, I. 1993. Analysis of 30 processing signals and study of transgene silencing in Nicotiana tabacum. Ph.D. thesis, Universiteit Gent, Gent, Belgium.

    Google Scholar 

  • Jakowitsch, J., Papp, I., Moscone, E.A., vanderWinden, J., Matzke, M. and Matzke, A.J.M. 1999. Molecular and cytogenetic characterization of a transgene locus that induces silencing and methylation of homologous promoters in trans. Plant J. 17: 131–140.

    PubMed  Google Scholar 

  • Jeddeloh, J.A., Stokes, T.L. and Richards, E.J. 1999. Maintenance of genomic methylation requires a SWI2/SNF2–like protein. Nature Genet. 22: 94–96.

    PubMed  Google Scholar 

  • Jones, A.L., Thomas, C.L.and Maule, A.J. 1998. De novo methylation and co-suppression induced by a cytoplasmically replicating plant RNA virus. EMBO J. 17: 6385–6393.

    PubMed  Google Scholar 

  • Jorgensen, R., Snyder, C. and Jones, J.D.G. 1987. T-DNA is organized predominantly in inverted repeat structures in plants transformed with Agrobacterium tumefaciens C58 derivates. Mol. Gen. Genet. 207: 471–477.

    Google Scholar 

  • Jorgensen, R., Cluster, P., Que, Q., English, J. and Napoli, C. 1996. Chalcone synthase cosuppression phenotypes in petunia flowers: comparison of sense vs. antisense constructs and single copy vs. complex T-DNA sequences. Plant Mol. Biol. 31: 957–973.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Ketting, R.F., Haverkamp, T.H.A., van Luenen, H.G.A.M. and Plasterk, R.H.A. 1999. mut-7 of C. elegans, required for transposon silencing and RNA interference, is a homolog of Werner syndrome helicase and RNaseD. Cell 99: 133–141.

    PubMed  Google Scholar 

  • Konokov, M., Bassuner, B. and Gelvin, S. 1997. Integration of T-DNA binary vector backbone sequences into the tobacco genome: evidence for multiple complex patterns of integration. Plant J. 11: 945–957.

    Article  PubMed  Google Scholar 

  • Kooter, J.M., Matzke, M.A. and Meyer, P. 1999. Listening to the silent genes: transgene silencing research identifies new mechanisms of gene regulation and pathogen control. Trends Plant Sci. 4: 340–347.

    PubMed  Google Scholar 

  • Kumagai, M.H., Donson, J., Dellacioppa, G., Harvey, D., Hanley, K. and Grill, L.K. 1995. Cytoplasmic inhibition of carotenoid biosynthesis with virus-derived RNA. Proc. Natl. Acad. Sci. USA 92: 1679–1683.

    PubMed  Google Scholar 

  • Leach, D.R.F. 1994. Long palindromes, cruciform structures, genetic instability and secondary structure repair. BioEssays 16: 893–900.

    PubMed  Google Scholar 

  • Leach, D.R.F. and Stahl, F.W. 1983. Viability of lambda phages carrying a perfect palindrome in the absence of recombination nucleases. Nature 305: 448–451.

    PubMed  Google Scholar 

  • Lilley, D.M.J. 1981. In vivo consequences of plasmid topology. Nature 292: 380–382.

    PubMed  Google Scholar 

  • Lindbo, J.A., Silva-Rosales, L., Proebsting, W.M. and Dougherty, W.G. 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.

    Article  PubMed  Google Scholar 

  • Lobachev, K.S., Shor, B.M., Tran, H.T., Taylor, W., Keen, J.D., Resnick, M.A. and Gordenin, D.A. 1998. Factors affecting inverted repeat stimulation of recombination and deletion in Saccharomyces cerevisiae. Genetics 148: 1507–1524.

    PubMed  Google Scholar 

  • Lloyd, R.G. and Buckman, C. 1985. Identification and genetic analysis of sbcC mutations in commonly used recBC sbcB strains of Escherichia coli K-12. J. Bact. 164: 836–844.

    PubMed  Google Scholar 

  • Luff, B., Pawlowski, L. and Bender, J. 1999. An inverted repeat triggers cytosine methylation of identical sequences in Arabidopsis. Mol. Cell 3: 505–511.

    Article  PubMed  Google Scholar 

  • Martienssen, R. 1996. Epigenetic phenomena: paramutation and gene silencing in plants. Curr. Biol. 6: 810–813.

    Google Scholar 

  • Matzke, M.A. and Matzke, A.J.M. 1998. Epigenetic silencing of plant transgenes as a consequence of diverse cellular defence responses. Cell. Mol. Life Sci. 54: 94–103.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Matzke, M.A., Matzke, A.J.M. and Eggelston, W.B. 1996. Paramutation and transgene silencing: a common response to invasive DNA? Trends Plant Sci. 1: 382–388.

    Google Scholar 

  • Mette, M.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.

    PubMed  Google Scholar 

  • Meyer, P., Heidmann, I. and Niedenhof, I. 1993. Differences in DNA-methylation are associated with a paramutation phenomenon in transgenic petunia. Plant J. 4: 89–100.

    PubMed  Google Scholar 

  • Meyer, P., Niedenhof, I. and ten Lohuis, M. 1994. Evidence for cytosine methylation of non-symmetrical sequences in transgenic Petunia hybrida. EMBO J. 13: 2084–2088.

    PubMed  Google Scholar 

  • Meyer, P. and Saedler, H. 1996. Homology-dependent gene silencing in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47: 23–48.

    PubMed  Google Scholar 

  • Montgomery, M.K., Xu, S.Q. and Fire, A. 1998. RNA as a target of double-stranded RNA-mediated genetic interference in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 95: 15502–15507.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Ngô, H., Tschudi, C., Gull, K. and Ullu, E. 1998. Double-stranded RNA induces mRNA degradation in Trypanosoma brucei. Proc. Natl. Acad. Sci. USA 95: 14687–14692.

    PubMed  Google Scholar 

  • Palauqui, J.C. and Balzergue, S. 1999. Activation of systemic acquired silencing by localised introduction of DNA. Curr. Biol. 9: 59–66.

    PubMed  Google Scholar 

  • Park, Y-D., Papp, I., Moscone, E.A., Iglesias, V.A., Vaucheret, H., Matzke, A.J.M. and Matzke, M.A. 1996. Gene silencing mediated by promoter homology occurs at the level of transcription and results in meiotically heritable alterations in methylation and gene activity. Plant J. 9: 183–194.

    PubMed  Google Scholar 

  • Pawlowski, W.P. and Somers, D.A. 1998. Transgenic DNA integrated into the oat genome is frequently interspersed by host DNA. Proc. Natl. Acad. Sci. USA 95: 12106–12110.

    PubMed  Google Scholar 

  • Pélissier, T., Thalmeir, S., Kempe, D., Sanger, 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.

    PubMed  Google Scholar 

  • Que, Q.D., 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.

    PubMed  Google Scholar 

  • Rossignol, J.L. and Faugeron, G. 1995. MIP: an epigenetic gene silencing process in Ascobolus immersus. In: P. Meyer (Ed.) Gene Silencing in Higher Plants and Related Phenomena in Other Eukaryotes, Springer-Verlag, Berlin, pp. 179–191.

    Google Scholar 

  • Ruiz, M.T., Voinnet, O. and Baulcombe, D.C. 1998. Initiation and maintenance of virus-induced gene silencing. Plant Cell 10: 937–946.

    PubMed  Google Scholar 

  • Saedler, H. and Nevers, P. 1985. Transposition in plants: a molecular model. EMBO J. 4: 585–590.

    Google Scholar 

  • Sanchez Alvardo, A. and Newmark, P.A. 1999. Double-stranded RNA specifically disrupts gene expression during planarian regeneration. Proc. Natl. Acad. Sci. USA 96: 5049–5054.

    PubMed  Google Scholar 

  • Selker, E.U. 1993. Control of DNA methylation in fungi. In: J.P. Jost and H.P. Saluz (Eds.) DNA Methylation: Molecular Biology and Biological Significance, Birkhäuser Verlag, Basel, pp. 212–217.

    Google Scholar 

  • Selker, E.U. 1998. Trichostatin A causes selective loss of DNA methylation in Neurospora. Proc. Natl. Acad. Sci. USA 95: 9430–9535.

    PubMed  Google Scholar 

  • Selker, E.U. 1999. Gene silencing: repeats that count. Cell 97: 157–160.

    PubMed  Google Scholar 

  • Singer, M.J. and Selker, E.U. 1995. Genetic and epigenetic inactivation of repetitive sequences in Neurospora crassa: RIP, DNA methylation, and quelling. In: P. Meyer (Ed.) Gene Silencing in Higher Plants and Other Phenomena in Other Eukaryotes, Springer-Verlag, Berlin, pp. 165–178.

    Google Scholar 

  • Sijen, T. and Kooter, J.M. 2000. Post-transcriptional silencing: RNAs on the attack or on the defensive? BioEssays, in press.

  • Sijen, T., Wellink, J., Hiriart, J.B. and van Kammen, A. 1996. RNA-mediated virus resistance: role of repeated transgenes and delineation of targeted regions. Plant Cell 8: 2277–2294.

    PubMed  Google Scholar 

  • 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 

  • 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.

    PubMed  Google Scholar 

  • Stam, M., de Bruin, R., van Blokland, R., ten Hoorn, R.A.L., Mol, J.N.M. and Kooter, J.M. 2000. Distinct features of posttranscriptional gene silencing by antisense transgenes in single copy and inverted T-DNA repeat loci. Plant J. 21: 27–42.

    PubMed  Google Scholar 

  • Stinard, P.S., Robertson, D.S. and Schnable, P.S. 1993. Genetic isolation, cloning, and analysis of a mutator-induced, dominant antimorph of the maize amylose extender1 locus. Plant Cell 5: 1555–1566.

    Article  PubMed  Google Scholar 

  • Tabara, H., Sarkissian, M., Kelly, W.G., Fleenor, J., Grishok, A., Timmons, L., Fire, A. and Mello, C.C. 1999. The rde-1 gene, RNA interference, and transposon silencing in C. elegans. Cell 99: 123–132.

    PubMed  Google Scholar 

  • Tinland, B. 1996. The integration of T-DNA into plant genomes. Trends Plant Sci. 1: 178–184.

    Article  Google Scholar 

  • Todd, J.J. and Vodkin, L.O. 1996. Duplications that suppress and deletions that restore expression from a chalcone synthase multigene family. Plant Cell 8: 687–699.

    PubMed  Google Scholar 

  • Tran, H., Degtyareva, N., Gordenin, D. and Resnick, M.A. 1997. Altered replication and inverted repeats induce mismatch repairindependent recombination between highly divergent DNAs in yeast. Mol. Cell. Biol. 17: 1027–1036.

    PubMed  Google Scholar 

  • Trinh, T.Q. and Sinden, R.R. 1991. Preferential DNA secondary structure mutagenesis in the lagging strand of DNA replication in E. coli. Nature 352: 544–547.

    PubMed  Google Scholar 

  • van Blokland, R., van der Geest, N., Mol, J.N.M. and Kooter, J.M. 1994. Transgene-mediated suppression of chalcone synthase expression in Petunia hybrida results from an increase in RNA turnover. Plant J. 6: 861–877.

    Article  Google Scholar 

  • 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. Plant J. 12: 379–392.

    Google Scholar 

  • 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. [III] 316: 1471–1483.

    Google Scholar 

  • Vaucheret, H., Elmayan, T., Mourrain, P. and Palauqui, J-C. 1996. Analysis of a tobacco transgene locus that triggers both transcriptional and post-transcriptional silencing. In: Russo, V.E., Martienssen, R.A. and Riggs, A.D (Eds.) Epigenetic Mechanisms of Gene Regulation, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 403–414.

    Google Scholar 

  • Vaucheret, H., Béclin, C., Elmayan, T., Feuerbach, F., Godon, C., Morel, J-B., Mourrain, P., Palauqui, J-C. and Vernhettes, S. 1998. Transgene-induced gene silencing in plants. Plant J. 16: 651–659.

    PubMed  Google Scholar 

  • Vaucheret, H., Nussaume, L., Palauqui, J-C., Quillere, I. and Elmayan, T. 1997. A transcriptionally active state is required for post-transcriptional silencing (cosuppression) of nitrate reductase host genes and transgenes. Plant Cell 9: 1495–1504.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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: 1–5.

    PubMed  Google Scholar 

  • Wassenegger, M. and Pélissier, T. 1998. A model for RNA-mediated gene silencing in higher plants. Plant Mol. Biol. 37: 349–362.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Waterhouse, P.M., Graham, H.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.

    PubMed  Google Scholar 

  • Waterhouse, P.M., Smith, N.A. and Wang, M.B. 1999. Virus resistance and gene silencing: killing the messenger. Trends Plant Sci. 4: 452–457.

    PubMed  Google Scholar 

  • Wenck, A., Czako, M., Kanevski, I. and Marton, L. 1997. Frequent collinear long transfer of DNA inclusive of the whole binary vector during Agrobacterium-mediated transformation. Plant Mol. Biol. 34: 913–922.

    Article  PubMed  Google Scholar 

  • Wolffe, A.P. and Matzke, M.A. 1999. Epigenetics: regulation through repression. Science 286: 481–486.

    PubMed  Google Scholar 

  • Ye, F. and Signer, E.R. 1996. RIGS (repeat-induced gene silencing) in Arabidopsis is transcriptional and alters chromatin configuration. Proc. Natl. Acad. Sci. USA 93: 10881–10886.

    PubMed  Google Scholar 

  • Zupan, J.R. and Zambryski, P. 1995. Transfer of T-DNA from Agrobacterium to the plant cell. Plant Physiol. 107: 1041–1047.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Muskens, M.W., Vissers, A.P., Mol, J.N. et al. Role of inverted DNA repeats in transcriptional and post-transcriptional gene silencing. Plant Mol Biol 43, 243–260 (2000). https://doi.org/10.1023/A:1006491613768

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1006491613768

Navigation