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Gene Silencing-Based Disease Resistance

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Abstract

The definition of a disease is fundamentally difficult, even if one considers only genetically based diseases. In its broadest sense, disease can be defined as any deviation from the norm that results in a physiological disadvantage. Natural selection ensures that the norm for any given species is constantly changing. In addition, some disadvantages are latent and might only manifest under certain environmental conditions. Conversely, an apparent disadvantage can carry a benefit, for example, the disease sickle-cell anemia that is an advantage in malarial areas. Because of the difficulties in giving disease a precise definition, in this review, gene silencing-based disease resistance will be restricted to the description of gene inactivation processes that contribute to maintain the physical fitness of an organism. In this sense, we are concerned with the elimination of invasive nucleic acid expressing. In numerous organisms, a variety of severe diseases are caused by the attack of invasive nucleic acids such as viruses and retroviral or transposable elements. Organisms have developed diverse mechanisms to defend themselves against such attack that include immune responses and apoptosis. Fungi, plants, invertebrates and vertebrates also enlist gene silencing systems to counteract the harmful effects of invasive nucleic acids. In particular, plants that lack interferon and immune responses have established efficient transcriptional and post-transcriptional gene silencing systems. In this review, we describe how plants defend against invasive nucleic acids and focus on the continual evolutionary battle between plants and viruses. In addition, the importance of controlling transposon activity is outlined. Finally, gene silencing-related mechanisms of genomic imprinting and X-chromosome inactivation are discussed in the context of disease resistance.

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References

  • Al-Kaff NS, Covey SN, Kreike MM, Page AM, Pinder R and Dale PJ (1998) Transcriptional and posttranscriptional plant gene silencing in response to a pathogen. Science 279: 2113–2115.

    Google Scholar 

  • Alvarado AS and Newmark PA (1999) Double-stranded RNA specifically disrupts gene expression during planarian regeneration. P Natl Acad Sci USA 96: 5049–5054.

    Google Scholar 

  • Amasino RM, Powell ALT and Gordon MP (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.

    Google Scholar 

  • Anandalakshmi R, Marathe R, Ge X, Herr Jr JM, Mau C, Mallory A et al. (2000) A calmodulin-related protein that suppresses posttranscriptional gene silencing in plants. Science 290: 142–144.

    Google Scholar 

  • Assaad FF, Tucker KL and Signer ER (1993) Epigenetic repeat-induced gene silencing (RIGS) in Arabidopsis. Plant Mol Biol 22: 1067–1085.

    Google Scholar 

  • Bailey JA, Carrel L, Chakravarti A and Eichler EE (2000) Molecular evidence for a relationship between LINE-1 elements and X chromosome inactivation: The Lyon repeat hypothesis. P Natl Acad Sci USA 97: 6634–6639.

    Google Scholar 

  • Bastin P, Ellis K, Kohl L and Gull K (2000) Flagellum ontogeny in trypanosomes studied via an inherited and regulated RNA interference system. J Cell Sci 113: 3321–3328.

    Google Scholar 

  • Baulcombe DC (1996) Mechanisms of pathogen-derived resistance to viruses in transgenic plants. Plant Cell 8: 1833–1844.

    Google Scholar 

  • Baulcombe DC (1999) Fast forward genetics based on virus-induced gene silencing. Curr Opin Plant Biol 2: 109–113.

    Google Scholar 

  • Baulcombe DC and English JJ (1996) Ectopic pairing of homologous DNA and post-transcriptional gene silencing in transgenic plants. Curr Opin Biotech 7: 173–180.

    Google Scholar 

  • Bell AC and Felsenfeld G (2000) Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene. Nature 405: 482–485.

    Google Scholar 

  • Bernstein E, Caudy AA, Hammond SM and Hannon GJ (2001) Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409: 363–366.

    Google Scholar 

  • Bird AP (1995) Gene number, noise reduction and biological complexity. Trends Genet 11: 94–100.

    Google Scholar 

  • Bird A (2002) DNA methylation patterns and epigenetic memory. Gene Dev 16: 6–21.

    Google Scholar 

  • Bosher JM and Labouesse M (2000) RNA interference: Genetic wand and genetic watchdog. Nat Cell Biol 2: E31–E36.

    Google Scholar 

  • Brigneti G, Voinnet O, Li WX, Ji LH, Ding SW and Baulcombe DC (1998) Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana. EMBO J 17: 6739–6746.

    Google Scholar 

  • Carthew RW (2001) Gene silencing by double-stranded RNA. Curr Opin Cell Biol 13: 244–248.

    Google Scholar 

  • Chao W, Huynh KD, Spencer RJ, Davidow LS and Lee JT (2002) CTCF, a candidate trans-acting factor for X-inactivation choice. Science 295: 345–347.

    Google Scholar 

  • Clemson CM, McNeil JA, Willard H and Lawrence JB (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.

    Google Scholar 

  • Cogoni C (2001) Homology-dependent gene silencing mechanisms in fungi. Annu Rev Microbiol 55: 381–406.

    Google Scholar 

  • Cogoni C, Irelan JT, Schumacher M, Schmidhauser TJ, Selker EU 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.

    Google Scholar 

  • Covey SN, Al-Kaff NS, Langara A and Turner DS (1997) Plants combat infection by gene silencing. Nature 387: 781–827.

    Google Scholar 

  • Debrand E, Chureau C, Arnaud D, Avner P and Heard E (1999) Functional analysis of the DXPas34 locus, a 3′ regulator of Xist expression. Mol Cell Biol 19: 8513–8525.

    Google Scholar 

  • Ding B, Itaya A and Woo YM (1999) Plasmodesmata and cell-to-cell communication in plants. Int Rev Cytol 190: 251–316.

    Google Scholar 

  • Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K and Tuschl T (2001a) Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411: 494–498.

    Google Scholar 

  • Elbashir SM, Lendeckel W and Tuschl T (2001b) RNA interference is mediated by 21-and 22-nucleotide RNAs. Genes Dev 15: 188–200.

    Google Scholar 

  • Faugeron G (2000) Diversity of homology-dependent gene silencing strategies in fungi. Curr Opin Microbiol 3: 144–148.

    Google Scholar 

  • Finnegan DJ (1992) Transposable elements. In: Lindsley DL and Zimm GG (eds), The Genome of Drosophila melanogaster (pp. 1096–1107) Academic Press, NY.

    Google Scholar 

  • Fire A, Xu SQ, Montgomery MK, Kostas SA, Driver SE and Mello CC (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391: 806–811.

    Google Scholar 

  • Garrick D, Fiering S, Martin DIK and Whitelaw E (1998) Repeat-induced gene silencing in mammals. Nat Genet 18: 56–59.

    Google Scholar 

  • Gowher H and Jeltsch A (2001) Enzymatic properties of recombinant Dnmt3a methyltransferase from mouse: The enzyme modifies DNA in a non-progressive manner and also methylates non-CpG [correction of non-CpA] sites. J Mol Biol 309: 1201–1208.

    Google Scholar 

  • Gowher H, Leismann O and Jeltsch A (2000) DNA of Drosophila melanogaster contains 5-methylcytosine. EMBO J 19: 6918–6923.

    Google Scholar 

  • Grishok A, Tabara H and Mello CC (2000) Genetic requirements for inheritance of RNAi in C. elegans. Science 287: 2494–2497.

    Google Scholar 

  • Guo HS and Ding SW (2002) A viral protein inhibits long range signaling activity of the gene silencing signal. EMBO J 21: 398–407.

    Google Scholar 

  • Hamilton AJ and Baulcombe DC(1999) A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286: 950–952.

    Google Scholar 

  • Hammond SM, Bernstein E, Beach D and Hannon GJ (2000) An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature 404: 293–296.

    Google Scholar 

  • Hammond SM, Caudy AA and Hannon GJ (2001a) Gene silencing by double-stranded RNA. Nature 2: 110–119.

    Google Scholar 

  • Hammond SM, Boettcher S, Caudy AA, Kobayashi R and Hannon GJ (2001b) Argonaute2, a link between genetic and biochemical analyses of RNAi. Science 293: 1146–1150.

    Google Scholar 

  • Heard E, Lovell-Badge R and Avner P (1999) Anti-Xistentialism. Nat Genet 21: 343–344.

    Google Scholar 

  • Hepburn AG, Clarke LE, Pearson L and White J (1983) The role of cytosine methylation in the control of nopaline synthase gene expression in a plant tumor. J Mol Appl Genet 2: 315–329.

    Google Scholar 

  • Hsieh J and Fire A (2000) Recognition and silencing of repeated DNA. Annu Rev Genet 34: 187–204.

    Google Scholar 

  • Jensen S, Gassama MP and Heidmann T (1999) Taming of transposable elements by homology-dependent gene silencing. Nat Genet 21: 209–212.

    Google Scholar 

  • Jones L, Hamilton AJ, Voinnet O, Thomas CL, Maule AJ and Baul-combe DC (1999) RNA-DNA interactions and DNA methylation in post-transcriptional gene silencing. Plant Cell 11: 2291–2301.

    Google Scholar 

  • Jones L, Ratcliff F and Baulcombe DC (2001) RNA-directed transcriptional gene silencing in plants can be inherited independently of the RNA trigger and requires Met1 for maintenance. Curr Biol 11: 747–757.

    Google Scholar 

  • Jorgensen R (1990) Altered gene expression in plants due to trans interactions between homologous genes. Trends Biotechnol 8: 340–344.

    Google Scholar 

  • Kennerdell JR and Carthew RW (1998) Use of dsRNA-mediated genetic interference to demonstrate that frizzled and frizzled 2 act in the wingless pathway. Cell 95: 1017–1026.

    Google Scholar 

  • Ketting RF and Plasterk RHA (2000) A genetic link between co-suppression and RNA interference in C. elegans. Nature 404: 296–298.

    Google Scholar 

  • Ketting RF, Haverkamp THA, van Luenen HGAM and Plasterk RHA (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.

    Google Scholar 

  • Kumagai MH, Donson J, Della-Cioppa G, Harvey D, Hanley K and Grill LK (1995) Cytoplasmic inhibition of carotenoid biosynthesis with virus-derived RNA. P Natl Acad Sci USA 92: 1679–1683.

    Google Scholar 

  • Li WX and Ding SW (2001) Viral suppressors of RNA silencing. Curr Opin Biotech 12: 150–154.

    Google Scholar 

  • Li YX, Farrell MJ, Liu R, Mohanty N and Kirby ML (2000) Double-stranded RNA injection produces null phenotypes in Zebrafish. Dev Biol 217: 394–405.

    Google Scholar 

  • Lindbo JA, Silva-Rosales L, Proebsting WM and Dougherty WG (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.

    Google Scholar 

  • Lipardi C, Wei Q and Paterson BM (2001) RNAi as random degra-dative PCR: siRNA primers convert mRNA into dsRNAs that are degraded to generate new siRNAs. Cell 107: 297–307.

    Google Scholar 

  • Llave C, Kasschau KD and Carrington JC (2000) Virus-encoded suppressor of posttranscriptional gene silencing targets a maintenance step in the silencing pathway. P Natl Acad Sci USA 97: 13401–13406.

    Google Scholar 

  • Lohe AR and Chaudhury A (2002) Genetic and epigenetic processes in seed development. Curr Opin Plant Biol 5: 19–25.

    Google Scholar 

  • Lohmann JU, Endl I and Bosch TCG (1999) Silencing of developmental genes in Hydra. Dev Biol 214: 211–214.

    Google Scholar 

  • Lucy AP, Guo HS, Li WX and Ding SW (2000) Suppression of post-transcriptional gene silencing by a plant viral protein localized in the nucleus. EMBO J 19: 1672–1680.

    Google Scholar 

  • Luikenhuis S, Wutz A and Jaenisch R (2001) Antisense transcription through the Xist locus mediates Tsix function in embryonic stem cells. Mol Cell Biol 21: 8512–8520.

    Google Scholar 

  • Malik K and Brown KW (2000) Epigenetic gene deregulation in cancer. Brit J Cancer 83: 1583–1588.

    Google Scholar 

  • Mallory AC, Ely L, Smith TH, Marathe R, Anandalakshmi R, Fagard M et al. (2001) HC-Pro suppression of transgene silencing eliminates the small RNAs but not transgene methylation or the mobile signal. Plant Cell 13: 571–583.

    Google Scholar 

  • Matienssen R (1998) Transposon, DNA methylation and gene control. Trends Genet 14: 263–264.

    Google Scholar 

  • Matzke MA, Primig M, Trnovsky J and Matzke AJM(1989) Reversible methylation and inactivation of marker genes in sequentially transformed tobacco plants. EMBO J 8: 643–649.

    Google Scholar 

  • Matzke MA, Mette MF, Aufsatz W, Jakowitsch J and Matzke AJM (1999) Host defenses to parasitic sequences and the evolution of epigenetic control mechanisms. Genetica 107: 271–287.

    Google Scholar 

  • Matzke M, Matzke AJM and Kooter JM (2001a) RNA: Guiding gene silencing. Science 293: 1080–1083.

    Google Scholar 

  • Matzke MA, Matzke AJM, Pruss GJ and Vance VB (2001b) RNA-based silencing strategies in plants. Curr Opin Genet Dev 11: 221–227.

    Google Scholar 

  • Mette F, Aufsatz W, van der Winden J, Matzke MA and Matzke AJM (2000) Transcriptional silencing and promoter methylation triggered by double-stranded RNA. EMBO J 19: 5194–5201.

    Google Scholar 

  • Meyer P and Saedler H (1996) Homology-dependent gene silencing in plants. Annu Rev Plant Phys 47: 23–48.

    Google Scholar 

  • Mittelsten Scheid O and Paszkowski J (2000) Transcriptional gene silencing mutants. Plant Mol Biol 43: 235–241.

    Google Scholar 

  • Miura A, Yonebayashi S, Watanabe K, Toyama T, Shimadak H and Kakutani T (2001) Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis. Nature 411: 212–214.

    Google Scholar 

  • Moazed D (2001) Common themes in mechanisms of gene silencing. Mol Cell 8: 489–498.

    Google Scholar 

  • Murfett J, Wang XJ, Hagen G and Guilfoyle TJ (2001) Identification of Arabidopsis histone deacetylase HDA6 mutants that affect transgene expression. Plant Cell 13: 1047–1061.

    Google Scholar 

  • Muskens MWM, Vissers APA, Mol JNM and Kooter JM (2000) Role of inverted DNA repeats in transcriptional and posttranscriptional gene silencing. Plant Mol Biol 43: 243–260.

    Google Scholar 

  • Napoli C, Lemieux C and Jorgensen R (1990) Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans. Plant Cell 2: 279–289.

    Google Scholar 

  • Nykänen A, Haley B and Zamore PD (2001) ATP requirements and small interfering RNA structure in the RNA interference pathway. Cell 107: 309–321.

    Google Scholar 

  • Okamoto H and Hirochika H (2001) Silencing of transposable elements in plants. Trends Plant Sci 6: 527–534.

    Google Scholar 

  • Oparka KJ and Santa Cruz S (2000) The great escape: Phloem transport and unloading of macromolecules. Annu Rev Plant Phys 51: 323–347.

    Google Scholar 

  • Palauqui JC and Balzergue S (1999) Activation of systemic silencing by localised introduction of DNA. Curr Biol 9: 59–66.

    Google Scholar 

  • Palauqui JC, Elmayan T, Pollien JM and Vaucheret H (1997) Systemic acquired silencing: Transgene-specific post-transcriptional silencing is transmitted by grafting from silenced stocks to non-silenced scions. EMBO J 16: 4738–4745.

    Google Scholar 

  • Pal-Bhadra M, Bhadra U and Birchler JA (1999) Cosuppression of nonhomologous transgenes in Drosophila involves mutually related endogenous sequences. Cell 99: 35–46.

    Google Scholar 

  • Papaefthimiou I, Hamilton AJ, Denti MA, Baulcombe DC, Tsagris M and Tabler M (2001) Replicating potato spindle tuber viroid RNA is accompanied by short RNA fragments that are characteristic of post-transcriptional gene silencing. Nucleic Acids Res 29: 2395–2400.

    Google Scholar 

  • Paszkowski J and Whitham SA (2001) Gene silencing and DNA methylation processes. Curr Opin Plant Biol 4: 123–129.

    Google Scholar 

  • Pélissier T, Thalmeir S, Kempe D, Sänger HL and Wassenegger M (1999) Heavy de novo methylation at symmetrical and non-symmetrical sites is a hallmark of RNA-directed DNA methylation. Nucleic Acids Res 27: 1625–1634.

    Google Scholar 

  • Prins M and Goldbach R (1996) RNA-mediated virus resistance in transgenic plants. Arch Virol 141: 2259–2276.

    Google Scholar 

  • Que Q, Wang HY, English JJ and Jorgensen RA (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.

    Google Scholar 

  • Ramsahoye BH, Biniszkiewicz D, Lyko F, Clark V, Bird AP and Jaenisch R (2000) Non-CpG methylation is prevalent in embryonic stem cells and may be mediated by DNA methyltransferase 3a. P Natl Acad Sci USA 97: 5237–5242.

    Google Scholar 

  • Ratcliff F, Harrison B and Baulcombe DC (1997) A similarity between viral defense and gene silencing in plants. Science 276: 1558–1560.

    Google Scholar 

  • Reik Wand Walter J (2001) Genomic imprinting: Parental influence on the genome. Nat Rev Genet 2: 21–32.

    Google Scholar 

  • Richards EJ (1997) DNA methylation and plant development. Trends Genet 13: 319–323.

    Google Scholar 

  • Ryner LC and Swain A (1995) Sex in the '90s. Cell 81: 483–493.

    Google Scholar 

  • Sado T, Fenner MH, Tan SS, Tam P, Shioda T and Li E (2000) X inactivation in the mouse embryo deficient for Dnmt1:Distinct effect of hypomethylation on imprinted and random X inactivation. Dev Biol 225: 294–303.

    Google Scholar 

  • SanMiguel P, Tikhonov A, Jin YK, Melake-Berhan A, Springer PS, Edwards KJ et al. (1996) Nested retrotransposons in the intergenic regions of the maize genome. Science 274: 765–768.

    Google Scholar 

  • Schiebel W, Pélissier T, Riedel L, Thalmeir S, Schiebel R, Kempe D et al. (1998) Isolation of a RNA-directed RNA polymerase-specific cDNA clone from tomato leaf-tissue mRNA. Plant Cell 10: 2087–2101.

    Google Scholar 

  • Schweizer P, Pokorny J, Schulze-Lefert P and Dudler R (2000) Double-stranded RNA interferes with gene function at the single-cell level in cereals. Plant J 24: 895–903.

    Google Scholar 

  • Sharp PA (2001) RNA interference - 2001. Gene Dev 15: 485–490.

    Google Scholar 

  • Sijen T and Kooter JM (2000) Post-transcriptional gene-silencing: RNAs on the attack or on the defense? BioEssays 22: 520–531.

    Google Scholar 

  • Sijen T, Vijn I, Rebocho A, van Blokland R, Roelofs D, Mol JNM et al. (2001a) Transcriptional and posttranscriptional gene silencing are mechanistically related. Curr Biol 11: 436–440.

    Google Scholar 

  • Sijen T, Fleenor J, Simmer F, Thijssen KL, Parrish S, Timmons L et al. (2001b) On the role of RNA amplification in dsRNA-triggered gene silencing. Cell 107: 465–476.

    Google Scholar 

  • Singer T, Yordan C and Martienssen RA (2001) Robertson's mutator transposons in A. thaliana are regulated by the chromatin-remodeling gene decrease in DNA methylation (DDM1). Gene Dev 15: 591–602.

    Google Scholar 

  • Sleutels F, Zwart R and Barlow DP ( 2002) The non-coding Air RNA is required for silencing autosomal imprinted genes. Nature 415: 810–813.

    Google Scholar 

  • Smith A (1996) The origin of interspersed repeats in the human genome. Curr Opin Genet Dev 6: 743–748.

    Google Scholar 

  • Spielman M, Vinkenoog R, Dickinson HG and Scott RJ (2001) The epigenetic basis of gender in flowering plants and mammals. Trends Genet 17: 705–711.

    Google Scholar 

  • Stark-Lorenzen P, Guitton MC, Werner R and Mühlbach HP (1997) Detection and tissue distribution of potato spindle tuber viroid in infected tomato plants by tissue print hybridisation. Arch Virol 142: 1289–1296.

    Google Scholar 

  • Steimer A, Amedeo P, Afsar K, Fransz P, Mittelsten Scheid O and Paszkowski J (2000) Endogenous targets of transcriptional gene silencing in Arabidopsis. Plant Cell 12: 1165–1178.

    Google Scholar 

  • Tabara H, Sarkissian M, Kelly WG, Fleenor J, Grishok A, Timmons L et al. (1999) The rde-1 gene, RNA interference, and transposon silencing in C. elegans. Cell 99: 123–132.

    Google Scholar 

  • Tuschl T (2001) RNA interference and small interfering RNAs. Chembiochem 2: 239–245.

    Google Scholar 

  • Van der Krol AR, Mur LA, Beld M, Mol JNM and Stuitje AR (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.

    Google Scholar 

  • Vaucheret H, Béclin C and Fagard M (2001) Post-transcriptional gene silencing in plants. J Cell Sci 114: 3083–3091.

    Google Scholar 

  • Voinnet O, Vain P, Angell S and Baulcombe D (1998) Systemic spread of sequence-specific transgene RNA degradation in plants is initiated by localized introduction of ectopic promoterless DNA. Cell 95: 177–187.

    Google Scholar 

  • Voinnet O, Pinto YM and Baulcombe DC (1999) Suppression of gene silencing: A general strategy used by diverse DNA and RNA viruses of plants. P Natl Acad Sci USA 96: 14147–14152.

    Google Scholar 

  • Voinnet O, Lederer C and Baulcombe DC (2000) A viral movement protein prevents spread of the gene silencing signal in Nicotiana benthamiana. Cell 103: 157–167.

    Google Scholar 

  • Voytas DF and Naylor GG (1998) Rapid flux in plant genomes. Nat Genet 20: 349–362.

    Google Scholar 

  • Walsh CP, Chaillet JR and Bestor TH (1998) Transcription of IAP endogenous retroviruses is constrained by cytosine methylation. Nat Genet 20: 116–117.

    Google Scholar 

  • Wassenegger M (2000) RNA-directed DNA methylation. Plant Mol Biol 43: 203–220.

    Google Scholar 

  • Wassenegger M (2002) Gene silencing. Int Rev Cytol 219: 61–113.

    Google Scholar 

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

    Google Scholar 

  • Wassenegger M, Heimes S, Riedel L and Sänger HL (1994) RNA-directed de novo methylation of genomic sequences in plants. Cell 76: 567–576.

    Google Scholar 

  • Waterhouse PM, Graham MW and Wang MB (1998) Virus resist-ance and gene silencing in plants can be induced by simultaneous expression of sense and antisense RNA. P Natl Acad Sci USA 95: 13959–13964.

    Google Scholar 

  • Waterhouse PM, Wang MB and Lough (2001a) Gene silencing as an adaptive defence against viruses. Nature 411: 834–842.

    Google Scholar 

  • Waterhouse PM, Wang MB and Finnegan EJ (2001b) Role of short RNAs in gene silencing. Trends Plant Sci 6: 297–301.

    Google Scholar 

  • WHO (1946) Preamble to the Constitution of the World Health Organization as adopted by the International Health Conference, New York, 19-22 June, 1946; signed on 22 July 1946 by the representatives of 61 States. Official Records of the World Health Organization 2: 100.

    Google Scholar 

  • Wianny F and Zernicka-Goetz M (2000) Specific interference with gene function by double-stranded RNA in early mouse development. Nat Cell Biol 2: 70–75.

    Google Scholar 

  • Wu-Scharf D, Jeong B, Zhang C and Cerutti H (2000) Transgene and transposon silencing in Chlamydomonas reinhardtii by a DEAH-box RNA helicase. Science 290: 1159–1162.

    Google Scholar 

  • Wutz A and Jaenisch R (2000) A shift from reversible to irreversible X inactivation is triggered during ES cell differentiation. Mol Cell 5: 695–705.

    Google Scholar 

  • Yoder JA, Walsh CP and Bestor TH (1997) Cytosine methylation and ecology of intragenomic parasites. Trends Genet 13: 335–340.

    Google Scholar 

  • Zambryski P and Crawford K (2000) Plasmodesmata: Gatekeepers for cell-to-cell transport of developmental signals in plants. Annu Rev Cell Dev Bi 16: 393–421.

    Google Scholar 

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Wassenegger, M. Gene Silencing-Based Disease Resistance. Transgenic Res 11, 639–653 (2002). https://doi.org/10.1023/A:1021130127700

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