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Gene Silencing in Plants: Transgenes as Targets and Effectors

  • Andreas E. MüllerEmail author
Chapter
Part of the Biotechnology in Agriculture and Forestry book series (AGRICULTURE, volume 64)

Abstract

Plant transformation is a versatile method to introduce or alter a trait-of-interest through expression of a transgene or through transgene-induced mutation and/or expression changes of endogenes. Transgenes in plants, however, are subject to gene-silencing effects that are an obstacle to stable and heritable expression of transgene-encoded traits. In an exciting twist, natural gene-silencing processes have been harnessed by researchers to achieve highly specific and targeted down-regulation of endogenous or pathogen-derived genes for functional studies, crop protection and crop improvement. Part 1 of this chapter attempts to give an overview of the mechanistic pillars of gene silencing in plants. Part 2 summarizes the factors that may cause unintended silencing of transgene expression, with practical advice on how to minimize the risk of transgene silencing. Part 3 addresses the intentional use of gene silencing for biotechnological applications in transgenic plants, with particular emphasis on RNA interference approaches.

Keywords

Inverted Repeat Natural Antisense Transcript Cryptic Promoter Chromosomal Integration Site Matrix Attachment Region Element 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Allen GC, Spiker S, Thompson WF (2000) Use of matrix attachment regions (MARs) to minimize transgene silencing. Plant Mol Biol 43:361–376PubMedCrossRefGoogle Scholar
  2. Allen RS, Millgate AG, Chitty JA, Thisleton J, Miller JA, Fist AJ, Gerlach WL, Larkin PJ (2004) RNAi-mediated replacement of morphine with the nonnarcotic alkaloid reticuline in opium poppy. Nat Biotechnol 22:1559–1566PubMedCrossRefGoogle Scholar
  3. Assaad FF, Tucker KL, Signer ER (1993) Epigenetic repeat-induced gene silencing (RIGS) in Arabidopsis. Plant Mol Biol 22:1067–1085PubMedCrossRefGoogle Scholar
  4. Baum JA, Bogaert T, Clinton W, Heck GR, Feldmann P, Ilagan O, Johnson S, Plaetinck G, Munyikwa T, Pleau M, Vaughn T, Roberts J (2007) Control of coleopteran insect pests through RNA interference. Nat Biotechnol 25:1322–1326PubMedCrossRefGoogle Scholar
  5. Borsani O, Zhu J, Verslues PE, Sunkar R, Zhu JK (2005) Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell 123:1279–1291PubMedCrossRefGoogle Scholar
  6. Brodersen P, Voinnet O (2006) The diversity of RNA silencing pathways in plants. Trends Genet 22:268–280PubMedCrossRefGoogle Scholar
  7. Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto YY, Sieburth L, Voinnet O (2008) Widespread translational inhibition by plant miRNAs and siRNAs. Science 320:1185–1190PubMedCrossRefGoogle Scholar
  8. Brummell DA, Balint-Kurti PJ, Harpster MH, Palys JM, Oeller PW, Gutterson N (2003) Inverted repeat of a heterologous 3'-untranslated region for high-efficiency, high-throughput gene silencing. Plant J 33:793–800PubMedCrossRefGoogle Scholar
  9. Bucher E, Lohuis D, van Poppel PMJA, Geerts-Dimitriadou C, Goldbach R, Prins M (2006) Multiple virus resistance at a high frequency using a single transgene construct. J Gen Virol 87:3697–3701PubMedCrossRefGoogle Scholar
  10. Butaye KM, Goderis IJ, Wouters PF, Pues JM, Delaure SL, Broekaert WF, Depicker A, Cammue BP, De Bolle MF (2004) Stable high-level transgene expression in Arabidopsis thaliana using gene silencing mutants and matrix attachment regions. Plant J 39:440–449PubMedCrossRefGoogle Scholar
  11. Butaye KMJ, Cammue BPA, Delaure SL, De Bolle MFC (2005) Approaches to minimize variation of transgene expression in plants. Mol Breed 16:79–91CrossRefGoogle Scholar
  12. Campbell MA, Fitzgerald HA, Ronald PC (2002) Engineering pathogen resistance in crop plants. Transgenic Res 11:599–613.PubMedCrossRefGoogle Scholar
  13. Candela H, Hake S (2008) The art and design of genetic screens: maize. Nat Rev Genet 9:192–203PubMedGoogle Scholar
  14. Chan SW (2008) Inputs and outputs for chromatin-targeted RNAi. Trends Plant Sci 13:383–389PubMedCrossRefGoogle Scholar
  15. Chan SW, Henderson IR, Jacobsen SE (2005) Gardening the genome: DNA methylation in Arabidopsis thaliana. Nat Rev Genet 6:351–360PubMedCrossRefGoogle Scholar
  16. Chapman EJ, Carrington JC (2007) Specialization and evolution of endogenous small RNA pathways. Nat Rev Genet 8:884–896PubMedCrossRefGoogle Scholar
  17. Chellappan P, Vanitharani R, Ogbe F, Fauquet CM (2005) Effect of temperature on geminivirus-induced RNA silencing in plants. Plant Physiol 138:1828–1841PubMedCrossRefGoogle Scholar
  18. Comai L, Henikoff S (2006) TILLING: practical single-nucleotide mutation discovery. Plant J 45:684–694PubMedCrossRefGoogle Scholar
  19. Dafny-Yelin M, Chung SM, Frankman EL, Tzfira T (2007) pSAT RNA interference vectors: a modular series for multiple gene down-regulation in plants. Plant Physiol 145:1272–1281PubMedCrossRefGoogle Scholar
  20. Davuluri GR, Tuinen A, Mustilli AC, Manfredonia A, Newman R, Burgess D, Brummell DA, King SR, Palys J, Uhlig J, Pennings HMJ, Bowler C (2004) Manipulation of DET1 expression in tomato results in photomorphogenic phenotypes caused by post-transcriptional gene silencing. Plant J 40:344–354PubMedCrossRefGoogle Scholar
  21. Davuluri GR, van Tuinen A, Fraser PD, Manfredonia A, Newman R, Burgess D, Brummell DA, King SR, Palys J, Uhlig J, Bramley PM, Pennings HMJ, Bowler C (2005) Fruit-specific RNAi-mediated suppression of DET1 enhances carotenoid and flavonoid content in tomatoes. Nat Biotechnol 23:890–895PubMedCrossRefGoogle Scholar
  22. Daxinger L, Kanno T, Bucher E, van der Winden J, Naumann U, Matzke AJ, Matzke M (2008) A stepwise pathway for biogenesis of 24-nt secondary siRNAs and spreading of DNA methylation. EMBO J 28:48–57PubMedCrossRefGoogle Scholar
  23. Day CD, Lee E, Kobayashi J, Holappa LD, Albert H, Ow DW (2000) Transgene integration into the same chromosome location can produce alleles that express at a predictable level, or alleles that are differentially silenced. Genes Dev 14:2869–2880PubMedCrossRefGoogle Scholar
  24. De Bolle MFC, Butaye KMJ, Coucke WJW, Goderis IJWM, Wouters PFJ, van Boxel N, Broekaert WF, Cammue BPA (2003) Analysis of the influence of promoter elements and a matrix attachment region on the inter-individual variation of transgene expression in populations of Arabidopsis thaliana. Plant Sci 165:169–179CrossRefGoogle Scholar
  25. De Bolle MF, Butaye KM, Goderis IJ, Wouters PF, Jacobs A, Delaure SL, Depicker A, Cammue BP (2007) The influence of matrix attachment regions on transgene expression in Arabidopsis thaliana wild type and gene silencing mutants. Plant Mol Biol 63:533–543PubMedCrossRefGoogle Scholar
  26. De Buck S, Windels P, De LM, Depicker A (2004) Single-copy T-DNAs integrated at different positions in the Arabidopsis genome display uniform and comparable beta-glucuronidase accumulation levels. Cell Mol Life Sci 61:2632–2645PubMedCrossRefGoogle Scholar
  27. De Haan P, Gielen JJ, Prins M, Wijkamp IG, Van SA, Peters D, van Grinsven MQ, Goldbach R (1992) Characterization of RNA-mediated resistance to tomato spotted wilt virus in transgenic tobacco plants. Biotechnology 10:1133–1137PubMedCrossRefGoogle Scholar
  28. De Wilde C, Podevin N, Windels P, Depicker A (2001) Silencing of antibody genes in plants with single-copy transgene inserts as a result of gene dosage effects. Mol Genet Genomics 265:647–653PubMedCrossRefGoogle Scholar
  29. Dennis ES, Peacock WJ (2007) Epigenetic regulation of flowering. Curr Opin Plant Biol 10:520–527PubMedCrossRefGoogle Scholar
  30. Di Nicola-Negri E, Brunetti A, Tavazza M, Ilardi V (2005) Hairpin RNA-mediated silencing of plum pox virus P1 and HC-Pro genes for efficient and predictable resistance to the virus. Transgenic Res 14:989–994PubMedCrossRefGoogle Scholar
  31. Ding SW, Voinnet O (2007) Antiviral immunity directed by small RNAs. Cell 130:413–426PubMedCrossRefGoogle Scholar
  32. Eamens A, Wang MB, Smith NA, Waterhouse PM (2008a) RNA silencing in plants: yesterday, today, and tomorrow. Plant Physiol 147:456–468PubMedCrossRefGoogle Scholar
  33. Eamens A, Vaistij FE, Jones L (2008b) NRPD1a and NRPD1b are required to maintain post-transcriptional RNA silencing and RNA-directed DNA methylation in Arabidopsis. Plant J 55:596–606PubMedCrossRefGoogle Scholar
  34. Eike MC, Mercy IS, Aalen RB (2005) Transgene silencing may be mediated by aberrant sense promoter sequence transcripts generated from cryptic promoters. Cell Mol Life Sci 62:3080–3091PubMedCrossRefGoogle Scholar
  35. Elmayan T, Vaucheret H (1996) Expression of single copies of a strongly expressed 35S transgene can be silenced post-transcriptionally. Plant J 9:787–797CrossRefGoogle Scholar
  36. Elmayan T, Balzergue S, Beon F, Bourdon V, Daubremet J, Guenet Y, Mourrain P, Palauqui JC, Vernhettes S, Vialle T, Wostrikoff K, Vaucheret H (1998) Arabidopsis mutants impaired in cosuppression. Plant Cell 10:1747–1758PubMedGoogle Scholar
  37. Escobar MA, Civerolo EL, Summerfelt KR, Dandekar AM (2001) RNAi-mediated oncogene silencing confers resistance to crown gall tumorigenesis. Proc Natl Acad Sci USA 98:13437–13442PubMedCrossRefGoogle Scholar
  38. Fairbairn DJ, Cavallaro AS, Bernard M, Mahalinga-Iyer J, Graham MW, Botella JR (2007) Host-delivered RNAi: an effective strategy to silence genes in plant parasitic nematodes. Planta 226:1525–1533PubMedCrossRefGoogle Scholar
  39. Finnegan EJ, Sheldon CC, Jardinaud F, Peacock WJ, Dennis ES (2004) A cluster of Arabidopsis genes with a coordinate response to an environmental stimulus. Curr Biol 14:911–916PubMedCrossRefGoogle Scholar
  40. Fire A, Xu SQ, Montgomery MK, Kostas SA, Driver SE, Mello CC (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806–811PubMedCrossRefGoogle Scholar
  41. Fischer U, Kuhlmann M, Pecinka A, Schmidt R, Mette MF (2008) Local DNA features affect RNA-directed transcriptional gene silencing and DNA methylation. Plant J 53:1–10PubMedCrossRefGoogle Scholar
  42. Fojtova M, Bleys A, Bedrichova J, Van HH, Krizova K, Depicker A, Kovarik A (2006) The trans-silencing capacity of invertedly repeated transgenes depends on their epigenetic state in tobacco. Nucleic Acids Res 34:2280–2293PubMedCrossRefGoogle Scholar
  43. Francis KE, Spiker S (2005) Identification of Arabidopsis thaliana transformants without selection reveals a high occurrence of silenced T-DNA integrations. Plant J 41:464–477PubMedCrossRefGoogle Scholar
  44. Fusaro AF, Matthew L, Smith NA, Curtin SJ, Dic-Hagan J, Ellacott GA, Watson JM, Wang MB, Brosnan C, Carroll BJ, Waterhouse PM (2006) RNA interference-inducing hairpin RNAs in plants act through the viral defence pathway. EMBO Rep 7:1168–1175PubMedCrossRefGoogle Scholar
  45. Gendler K, Paulsen T, Napoli C (2008) ChromDB: the chromatin database. Nucleic Acids Res 36:D298–D302PubMedCrossRefGoogle Scholar
  46. Girard A, Hannon GJ (2008) Conserved themes in small-RNA-mediated transposon control. Trends Cell Biol 18:136–148PubMedCrossRefGoogle Scholar
  47. Grant-Downton RT, Dickinson HG (2005) Epigenetics and its implications for plant biology. 1. The epigenetic network in plants. Ann Bot 96:1143–1164PubMedCrossRefGoogle Scholar
  48. Hamilton AJ, Baulcombe DC (1999) A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286:950–952PubMedCrossRefGoogle Scholar
  49. Hebert CG, Valdes JJ, Bentley WE (2008) Beyond silencing -- engineering applications of RNA interference and antisense technology for altering cellular phenotype. Curr Opin Biotechnol 19:500–505PubMedCrossRefGoogle Scholar
  50. Helliwell CA, Waterhouse PM (2005) Constructs and methods for hairpin RNA-mediated gene silencing in plants. RNA Interfer 392:24–35CrossRefGoogle Scholar
  51. Henderson IR, Jacobsen SE (2007) Epigenetic inheritance in plants. Nature 447:418–424PubMedCrossRefGoogle Scholar
  52. Hobbs SL, Kpodar P, DeLong CM (1990) The effect of T-DNA copy number, position and methylation on reporter gene expression in tobacco transformants. Plant Mol Biol 15:851–864PubMedCrossRefGoogle Scholar
  53. Hollick JB (2008) Sensing the epigenome. Trends Plant Sci 13:398–404PubMedCrossRefGoogle Scholar
  54. Houmard NM, Mainville JL, Bonin CP, Huang S, Luethy MH, Malvar TM (2007) High-lysine corn generated by endosperm-specific suppression of lysine catabolism using RNAi. Plant Biotechnol J 5:605–614PubMedCrossRefGoogle Scholar
  55. Huang X, Han Y, Wiig A, McMillan J, Jones T, Talton W, Dong J, Offenheiser M, Ren P, Ascenzi R, Hill S, Zhen R, Chaudhuri S (2006) Engineering resistance against plant-parasitic nematodes. J Nematol 38:275Google Scholar
  56. Huettel B, Kanno T, Daxinger L, Bucher E, van der Winden J, Matzke AJM, Matzke M (2007) RNA-directed DNA methylation mediated by DRD1 and Pol IVb: A versatile pathway for transcriptional gene silencing in plants. Biochim Biophys Acta -- Gene Struct Express 1769:358–374CrossRefGoogle Scholar
  57. Jakowitsch J, Papp I, Moscone EA, van der Winden J, Matzke M, Matzke AJM (1999) Molecular and cytogenetic characterization of a transgene locus that induces silencing and methylation of homologous promoters in trans. Plant J 17:131–140PubMedCrossRefGoogle Scholar
  58. Jan FJ, Fagoaga C, Pang SZ, Gonsalves D (2000) A single chimeric transgene derived from two distinct viruses confers multi-virus resistance in transgenic plants through homology-dependent gene silencing. J Gen Virol 81:2103–2109PubMedGoogle Scholar
  59. Jiang D, Yang W, He Y, Amasino RM (2007) Arabidopsis relatives of the human lysine-specific demethylase1 repress the expression of FWA and FLOWERING LOCUS C and thus promote the floral transition. Plant Cell 19:2975–2987PubMedCrossRefGoogle Scholar
  60. Jin H, Vacic V, Girke T, Lonardi S, Zhu JK (2008) Small RNAs and the regulation of cis-natural antisense transcripts in Arabidopsis. BMC Mol Biol 9:6PubMedCrossRefGoogle Scholar
  61. Jones JDG, Gilbert DE, Grady KL, Jorgensen RA (1987) T-DNA structure and gene expression in petunia plants transformed by Agrobacterium tumefaciens C58 derivatives. Mol Gen Genet 207:478–485CrossRefGoogle Scholar
  62. Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAS and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53PubMedCrossRefGoogle Scholar
  63. Jorgensen RA (2003) Sense cosuppression in plants: past, present, and future. In: Hannon GJ (ed) RNAi: a guide to gene silencing. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y., pp 5–21Google Scholar
  64. Jorgensen RA, Cluster PD, English J, Que Q, Napoli CA (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 31:957–973PubMedCrossRefGoogle Scholar
  65. Jorgensen RA, Doetsch N, Muller A, Que Q, Gendler K, Napoli CA (2007) A paragenetic perspective on integration of RNA silencing into the epigenome and its role in the biology of higher plants. Cold Spring Harbor Symp Quant Biol 71:481–485CrossRefGoogle Scholar
  66. Jung KH, An G, Ronald PC (2008) Towards a better bowl of rice: assigning function to tens of thousands of rice genes. Nat Rev Genet 9:91–101PubMedGoogle Scholar
  67. Kanno T, Huettel B, Mette MF, Aufsatz W, Jaligot E, Daxinger L, Kreil DP, Matzke M, Matzke AJM (2005) Atypical RNA polymerase subunits required for RNA-directed DNA methylation. Nat Genet 37:761–765PubMedCrossRefGoogle Scholar
  68. Katiyar-Agarwal S, Morgan R, Dahlbeck D, Borsani O, Villegas A Jr, Zhu JK, Staskawicz BJ, Jin H (2006) A pathogen-inducible endogenous siRNA in plant immunity. Proc Natl Acad Sci USA 103:18002–18007PubMedCrossRefGoogle Scholar
  69. Kato M, Takashima K, Kakutani T (2004) Epigenetic control of CACTA transposon mobility in Arabidopsis thaliana. Genetics 168:961–969PubMedCrossRefGoogle Scholar
  70. Kim SI, Veena V, Gelvin SB (2007) Genome-wide analysis of Agrobacterium T-DNA integration sites in the Arabidopsis genome generated under non-selective conditions. Plant J 51:779–791PubMedCrossRefGoogle Scholar
  71. Kinoshita T, Miura A, Choi YH, Kinoshita Y, Cao XF, Jacobsen SE, Fischer RL, Kakutani T (2004) One-way control of FWA imprinting in Arabidopsis endosperm by DNA methylation. Science 303:521–523PubMedCrossRefGoogle Scholar
  72. Levin JS, Thompson WF, Csinos AS, Stephenson MG, Weissinger AK (2005) Matrix attachment regions increase the efficiency and stability of RNA-mediated resistance to tomato spotted wilt virus in transgenic tobacco. Transgenic Res 14:193–206PubMedCrossRefGoogle Scholar
  73. Lindbo JA, Dougherty WG (2005) Plant pathology and RNAi: a brief history. Annu Rev Phytopathol 43:191–204PubMedCrossRefGoogle Scholar
  74. Lippman Z, May B, Yordan C, Singer T, Martienssen R (2003) Distinct mechanisms determine transposon inheritance and methylation via small interfering RNA and histone modification. PLoS Biol 1:E67PubMedCrossRefGoogle Scholar
  75. Lippman Z, Gendrel AV, Black M, Vaughn MW, Dedhia N, McCombie WR, Lavine K, Mittal V, May B, Kasschau KD, Carrington JC, Doerge RW, Colot V, Martienssen R (2004) Role of transposable elements in heterochromatin and epigenetic control. Nature 430:471–476PubMedCrossRefGoogle Scholar
  76. Lunerova-Bedrichova J, Bleys A, Fojtova M, Khaitova L, Depicker A, Kovarik A (2008) Trans-generation inheritance of methylation patterns in a tobacco transgene following a post-transcriptional silencing event. Plant J 54:1049–1062PubMedCrossRefGoogle Scholar
  77. Luo KM, Harding SA, Tsai CJ (2008) A modified T-vector for simplified assembly of hairpin RNAi constructs. Biotechnol Lett 30:1271–1274PubMedCrossRefGoogle Scholar
  78. Ma C, Mitra A (2002) Intrinsic direct repeats generate consistent post-transcriptional gene silencing in tobacco. Plant J 31:37–49PubMedCrossRefGoogle Scholar
  79. Mallory AC, Elmayan T, Vaucheret H (2008) MicroRNA maturation and action -- the expanding roles of ARGONAUTEs. Curr Opin Plant Biol 11:560–566PubMedCrossRefGoogle Scholar
  80. Mao YB, Cai WJ, Wang JW, Hong GJ, Tao XY, Wang LJ, Huang YP, Chen XY (2007) Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nat Biotechnol 25:1307–1313PubMedCrossRefGoogle Scholar
  81. Matzke AJ, Matzke MA (1998) Position effects and epigenetic silencing of plant transgenes. Curr Opin Plant Biol 1:142–148PubMedCrossRefGoogle Scholar
  82. Matzke MA, Primig M, Trnovsky J, Matzke AJ (1989) Reversible methylation and inactivation of marker genes in sequentially transformed tobacco plants. EMBO J 8:643–649PubMedGoogle Scholar
  83. Matzke MA, Aufsatz W, Kanno T, Mette MF, Matzke AJ (2002) Homology-dependent gene silencing and host defense in plants. Adv Genet 46:235–275PubMedCrossRefGoogle Scholar
  84. Matzke MA, Kanno T, Huettel B, Daxinger L, Matzke AJM (2007) Targets of RNA-directed DNA methylation. Curr Opin Plant Biol 10:512–519PubMedCrossRefGoogle Scholar
  85. McGinnis K, Chandler V, Cone K, Kaeppler H, Kaeppler S, Kerschen A, Pikaard C, Richards E, Sidorenko L, Smith T, Springer N, Wulan T (2005) Transgene-induced RNA interference as a tool for plant functional genomics. RNA Interfer 392:1–24CrossRefGoogle Scholar
  86. Mette MF, van der Winden J, Matzke MA, Matzke AJ (1999) Production of aberrant promoter transcripts contributes to methylation and silencing of unlinked homologous promoters in trans. EMBO J 18:241–248PubMedCrossRefGoogle Scholar
  87. Mette MF, Aufsatz W, van der Winden J, Matzke MA, Matzke AJ (2000) Transcriptional silencing and promoter methylation triggered by double-stranded RNA. EMBO J 19: 5194–5201PubMedCrossRefGoogle Scholar
  88. Meyer S, Nowak K, Sharma VK, Schulze J, Mendel RR, Hansch R (2004) Vectors for RNAi technology in poplar. Plant Biol 6:100–103PubMedCrossRefGoogle Scholar
  89. Meza TJ, Stangeland B, Mercy IS, Skarn M, Nymoen DA, Berg A, Butenko MA, Hakelien AM, Haslekas C, Meza-Zepeda LA, Aalen RB (2002) Analyses of single-copy Arabidopsis T-DNA-transformed lines show that the presence of vector backbone sequences, short inverted repeats and DNA methylation is not sufficient or necessary for the induction of transgene silencing. Nucleic Acids Res 30:4556–4566PubMedCrossRefGoogle Scholar
  90. Miki D, Shimamoto K (2004) Simple RNAi vectors for stable and transient suppression of gene function in rice. Plant Cell Physiol 45:490–495PubMedCrossRefGoogle Scholar
  91. Mlotshwa S, Pruss GJ, Vance V (2008) Small RNAs in viral infection and host defense. Trends Plant Sci 13:375–382PubMedCrossRefGoogle Scholar
  92. Mlynarova L, Loonen A, Heldens J, Jansen RC, Keizer P, Stiekema WJ, Nap JP (1994) Reduced position effect in mature transgenic plants conferred by the chicken lysozyme matrix-associated region. Plant Cell 6:417–426PubMedGoogle Scholar
  93. Mlynarova L, Jansen RC, Conner AJ, Stiekema WJ, Nap JP (1995) The MAR-mediated reduction in position effect can be uncoupled from copy number-dependent expression in transgenic plants. Plant Cell 7:599–609PubMedGoogle Scholar
  94. Mourrain P, van Blokland R, Kooter JM, Vaucheret H (2007) A single transgene locus triggers both transcriptional and post-transcriptional silencing through double-stranded RNA production. Planta 225:365–379PubMedCrossRefGoogle Scholar
  95. Muller AE (2006) Applications of RNA interference in transgenic plants. CAB Rev Perspect Agric Vet Sci Nutr Nat Resour 1:1–13Google Scholar
  96. Muller AE, Wassenegger M (2004) Control and silencing of transgene expression. In: Christou PKH (ed) Handbook of plant biotechnology. Wiley, Chichester, pp 291–330Google Scholar
  97. Muskens MW, Vissers AP, Mol JN, Kooter JM (2000) Role of inverted DNA repeats in transcriptional and post-transcriptional gene silencing. Plant Mol Biol 43:243–260PubMedCrossRefGoogle Scholar
  98. Nagaya S, Kato K, Ninomiya Y, Horie R, Sekine M, Yoshida K, Shinmyo A (2005) Expression of randomly integrated single complete copy transgenes does not vary in Arabidopsis thaliana. Plant Cell Physiol 46:438–444PubMedCrossRefGoogle Scholar
  99. Obbard DJ, Gordon KH, Buck AH, Jiggins FM (2009) The evolution of RNAi as a defence against viruses and transposable elements. Philos Trans R Soc Lond B Biol Sci 364:99–115PubMedCrossRefGoogle Scholar
  100. Ogita S, Yamaguchi Y, Koizumi N, Sano H (2003) Supression of theobromine synthase gene by RNAi in coffee plants. Plant Cell Physiol 44:S88Google Scholar
  101. Ogita S, Uefuji H, Morimoto M, Sano H (2004) Application of RNAi to confirm theobromine as the major intermediate for caffeine biosynthesis in coffee plants with potential for construction of decaffeinated varieties. Plant Mol Biol 54:931–941PubMedCrossRefGoogle Scholar
  102. Ossowski S, Schwab R, Weigel D (2008) Gene silencing in plants using artificial microRNAs and other small RNAs. Plant J 53:674–690PubMedCrossRefGoogle Scholar
  103. Ostergaard L, Yanofsky MF (2004) Establishing gene function by mutagenesis in Arabidopsis thaliana. Plant J 39:682–696PubMedCrossRefGoogle Scholar
  104. Ow DW (2002) Recombinase-directed plant transformation for the post-genomic era. Plant Mol Biol 48:183–200PubMedCrossRefGoogle Scholar
  105. Petersen K, Leah R, Knudsen S, Cameron-Mills V (2002) Matrix attachment regions (MARs) enhance transformation frequencies and reduce variance of transgene expression in barley. Plant Mol Biol 49:45–58PubMedCrossRefGoogle Scholar
  106. Pfluger J, Wagner D (2007) Histone modifications and dynamic regulation of genome accessibility in plants. Curr Opin Plant Biol 10:645–652PubMedCrossRefGoogle Scholar
  107. Pikaard CS, Haag JR, Ream T, Wierzbicki AT (2008) Roles of RNA polymerase IV in gene silencing. Trends Plant Sci 13:390–397PubMedCrossRefGoogle Scholar
  108. Price DRG, Gatehouse JA (2008) RNAi-mediated crop protection against insects. Trends Biotechnol 26:393–400PubMedCrossRefGoogle Scholar
  109. Prins M, Laimer M, Noris E, Schubert J, Wassenegger M, Tepfer M (2008) Strategies for antiviral resistance in transgenic plants. Mol Plant Pathol 9:73–83PubMedGoogle Scholar
  110. Que Q, Wang HY, English JJ, 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 9:1357–1368PubMedGoogle Scholar
  111. Ramachandran V, Chen X (2008) Small RNA metabolism in Arabidopsis. Trends Plant Sci 13:368–374PubMedCrossRefGoogle Scholar
  112. Rommens CM, Haring MA, Swords K, Davies HV, Belknap WR (2007) The intragenic approach as a new extension to traditional plant breeding. Trends Plant Sci 12:397–403PubMedCrossRefGoogle Scholar
  113. Rommens CM, Yan H, Swords K, Richael C, Ye JS (2008) Low-acrylamide French fries and potato chips. Plant Biotechnol J 6:843–853PubMedCrossRefGoogle Scholar
  114. Schubert D, Lechtenberg B, Forsbach A, Gils M, Bahadur S, Schmidt R (2004) Silencing in Arabidopsis T-DNA transformants: the predominant role of a gene-specific RNA sensing mechanism versus position effects. Plant Cell 16:2561–2572PubMedCrossRefGoogle Scholar
  115. Schwab R, Ossowski S, Riester M, Warthmann N, Weigel D (2006) Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18:1121–1133PubMedCrossRefGoogle Scholar
  116. Segal G, Song RT, Messing J (2003) A new opaque variant of maize by a single dominant RNA-interference-inducing transgene. Genetics 165:387–397PubMedGoogle Scholar
  117. Sels J, Delaure SL, Aerts AM, Proost P, Cammue BPA, De Bolle MFC (2007) Use of a PTGS-MAR expression system for efficient in planta production of bioactive Arabidopsis thaliana plant defensins. Transgenic Res 16:531–538PubMedCrossRefGoogle Scholar
  118. Sindhu AS, Maier TR, Mitchum MG, Hussey RS, Davis EL, Baum TJ (2009) Effective and specific in planta RNAi in cyst nematodes: expression interference of four parasitism genes reduces parasitic success. J Exp Bot 60:315–324PubMedCrossRefGoogle Scholar
  119. Slade AJ, Knauf VC (2005) TILLING moves beyond functional genomics into crop improvement. Transgenic Res 14:109–115PubMedCrossRefGoogle Scholar
  120. Smith NA, Singh SP, Wang MB, Stoutjesdijk PA, Green AG, Waterhouse PM (2000) Gene expression -- total silencing by intron-spliced hairpin RNAs. Nature 407:319–320PubMedCrossRefGoogle Scholar
  121. Soppe WJ, Jacobsen SE, Onso-Blanco C, Jackson JP, Kakutani T, Koornneef M, Peeters AJ (2000) The late flowering phenotype of fwa mutants is caused by gain-of-function epigenetic alleles of a homeodomain gene. Mol Cell 6:791–802PubMedCrossRefGoogle Scholar
  122. Srivastava V, Riza-Nieto M, Wilson AJ (2004) Cre-mediated site-specific gene integration for consistent transgene expression in rice. Plant Biotechnol J 2:169–179PubMedCrossRefGoogle Scholar
  123. Sung S, Amasino RM (2005) Remembering winter: toward a molecular understanding of vernalization. Annu Rev Plant Biol 56:491–508PubMedCrossRefGoogle Scholar
  124. Sunilkumar G, Campbell LM, Puckhaber L, Stipanovic RD, Rathore KS (2006) Engineering cottonseed for use in human nutrition by tissue-specific reduction of toxic gossypol. Proc Natl Acad Sci USA 103:18054–18059PubMedCrossRefGoogle Scholar
  125. Swiezewski S, Crevillen P, Liu F, Ecker JR, Jerzmanowski A, Dean C (2007) Small RNA-mediated chromatin silencing directed to the 3' region of the Arabidopsis gene encoding the developmental regulator, FLC. Proc Natl Acad Sci USA 104:3633–3638CrossRefGoogle Scholar
  126. Taliansky M, Kim SH, Mayo MA, Kalinina NO, Fraser G, McGeachy KD, Barker H (2004) Escape of a plant virus from amplicon-mediated RNA silencing is associated with biotic or abiotic stress. Plant J 39:194–205PubMedCrossRefGoogle Scholar
  127. Tang GL, Galili G, Zhuang X (2007) RNAi and microRNA: breakthrough technologies for the improvement of plant nutritional value and metabolic engineering. Metabolomics 3:357–369CrossRefGoogle Scholar
  128. Townsend BJ, Llewellyn DJ (2007) Reduced terpene levels in cottonseed add food to fiber. Trends Biotechnol 25:239–241PubMedCrossRefGoogle Scholar
  129. Tzfira T, White C (2005) Towards targeted mutagenesis and gene replacement in plants. Trends Biotechnol 23:567–569PubMedCrossRefGoogle Scholar
  130. 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 -- Life Sci 316:1471–1483Google Scholar
  131. Vaucheret H, Elmayan T, Mourrain P, Palauqui JC (1996) Analysis of a tobacco transgene locus that triggers both transcriptional and post-transcriptional silencing. V.E. Russo, R.A. Martienssen, and A.D. Riggs (eds) Cold Spring Harbor Laboratory, pp. 403–414Google Scholar
  132. Voinnet O (2008) Use, tolerance and avoidance of amplified RNA silencing by plants. Trends Plant Sci 13:317–328PubMedCrossRefGoogle Scholar
  133. Wang H, Chua NH, Wang XJ (2006) Prediction of trans-antisense transcripts in Arabidopsis thaliana. Genome Biol 7:R92PubMedCrossRefGoogle Scholar
  134. Wang MB, Waterhouse PM (2000) High-efficiency silencing of a beta-glucuronidase gene in rice is correlated with repetitive transgene structure but is independent of DNA methylation. Plant Mol Biol 43:67–82PubMedCrossRefGoogle Scholar
  135. Wang XJ, Gaasterland T, Chua NH (2005) Genome-wide prediction and identification of cis-natural antisense transcripts in Arabidopsis thaliana. Genome Biol 6:R30PubMedCrossRefGoogle Scholar
  136. Warthmann N, Chen H, Ossowski S, Weigel D, Herve P (2008) Highly specific gene silencing by artificial miRNAs in rice. PLoS ONE 3:e1829PubMedCrossRefGoogle Scholar
  137. Wassenegger M, Krczal G (2006) Nomenclature and functions of RNA-directed RNA polymerases. Trends Plant Sci 11:142–151PubMedCrossRefGoogle Scholar
  138. Waterhouse PM, Graham HW, Wang MB (1998) Virus resistance and gene silencing in plants can be induced by simultaneous expression of sense and antisense RNA. Proc Natl Acad Sci USA 95:13959–13964PubMedCrossRefGoogle Scholar
  139. Wesley SV, Helliwell CA, Smith NA, Wang MB, Rouse DT, Liu Q, Gooding PS, Singh SP, Abbott D, Stoutjesdijk PA, Robinson SP, Gleave AP, Green AG, Waterhouse PM (2001) Construct design for efficient, effective and high-throughput gene silencing in plants. Plant J 27:581–590PubMedCrossRefGoogle Scholar
  140. Wielopolska A, Townley H, Moore I, Waterhouse P, Helliwell C (2005) A high-throughput inducible RNAi vector for plants. Plant Biotechnol J 3:583–590PubMedCrossRefGoogle Scholar
  141. Wierzbicki AT, Haag JR, Pikaard CS (2008) Noncoding transcription by RNA polymerase Pol IVb/Pol V mediates transcriptional silencing of overlapping and adjacent genes. Cell 135:635–648PubMedCrossRefGoogle Scholar
  142. Wu XL, Hou WC, Wang MM, Zhu XP, Li F, Zhang JD, Li XZ, Guo XQ (2008) RNA silencing-mediated resistance is related to biotic/abiotic stresses and cellular RdRp expression in transgenic tobacco plants. BMB Rep 41:376–381PubMedCrossRefGoogle Scholar
  143. Xu X, Zhu D, Zhao Q, Ao G, Ma C, Yu J (2009) RNA silencing mediated by direct repeats in maize: a potential tool for functional genomics. Mol Biotechnol 41:213–223PubMedCrossRefGoogle Scholar
  144. Yadav BC, Veluthambi K, Subramaniam K (2006) Host-generated double stranded RNA induces RNAi in plant-parasitic nematodes and protects the host from infection. Mol Biochem Parasitol 148:219–222PubMedCrossRefGoogle Scholar
  145. Yan H, Chretien R, Ye J, Rommens CM (2006) New construct approaches for efficient gene silencing in plants. Plant Physiol 141:1508–1518PubMedCrossRefGoogle Scholar
  146. Zhai J, Liu J, Liu B, Li P, Meyers BC, Chen X, Cao X (2008) Small RNA-directed epigenetic natural variation in Arabidopsis thaliana. PLoS Genet 4:e1000056PubMedCrossRefGoogle Scholar
  147. Zhang J, Lu L, Ji L, Yang G, Zheng C (2009) Functional characterization of a tobacco matrix attachment region-mediated enhancement of transgene expression. Transgenic Res 18:377–385PubMedCrossRefGoogle Scholar
  148. Zilberman D (2008) The evolving functions of DNA methylation. Curr Opin Plant Biol 11:554–559PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2010

Authors and Affiliations

  1. 1.Christian-Albrechts University of Kiel, Plant Breeding InstituteKielGermany

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