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RNA as a target and an initiator of post-transcriptional gene silencing in trangenic plants

  • RNA Processing and Stability
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Abstract

Post-transcriptional gene silencing in transgenic plants is the manifestation of a mechanism that suppresses RNA accumulation in a sequence-specific manner. The target RNA species may be the products of transgenes, endogenous plant genes or viral RNAs. For an RNA to be a target it is necessary only that it has sequence homology to the sense RNA product of the transgene. There are three current hypotheses to account for the mechanism of post transcriptional gene silencing. These models all require production of an antisense RNA of the RNA targets to account for the specificity of the mechanism. There could be either direct transcription of the antisense RNA from the transgene, antisense RNA produced in response to over expression of the transgene or antisense RNA produced in response to the production of an aberrant sense RNA product of the transgene. To determine which of these models is correct it will be necessary to find out whether transgene methylation, which is frequently associated with the potential of transgenes to confer post-transcriptional gene silencing, is a cause or a consequence of the process.

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References

  1. Angenent GC, Franken J, Busscher M, Weiss D, van Tunen AJ: Co-suppression of the petunia homeotic gene fbp2 affects the identity of the generative meristem. Plant J 5: 33–44 (1994).

    Google Scholar 

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

    Google Scholar 

  3. Barry C, Faugeron G, Rossignol J-L: Methylation induced premeiotically in Ascobulus: coextension with DNA repeat lengths and effect on transcript elongation. Proc Natl Acad Sci USA 90: 4557–4561 (1993).

    Google Scholar 

  4. Baulcombe DC: Replicase mediated resistance: a novel type of virus resistance in transgenic plants? Trends Microbiol 2: 60–63 (1994).

    Google Scholar 

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

  6. Boerjan W, Bauw G, Van Montagu M, Inzé D: Distinct phenotypes generated by overexpression and supression of S-adenosyl-L-methionine synthetase reveal developmental patterns of gene silencing in tobacco. Plant Cell 6: 1401–1414 (1994).

    Google Scholar 

  7. Brandle JE, Mchugh SG, James L, Labbe H, Miki BL: Instability of transgene expression in-field grown tobacco carrying the csrl-l gene for sulfonylurea herbicide resistance. Bio/technology 13: 994–998 (1995).

    Google Scholar 

  8. Day AG, Bejarano ER, Buck KW, Burrell M, Lichtenstein CP: Expression of an antisense viral gene in transgenic tobacco confers resistance to the DNA virus tomato golden mosaicvirus. Proc Natl Acad Sci USA 88: 6721–6725 (1991).

    Google Scholar 

  9. de Borne FD, Vincentz M, Chupeau Y, Vaucheret H: Cosuppression of nitrate reductase host genes and transgenes in transgenic tobacco plants. Mol Gen Genet 243: 613–621 (1994).

    Google Scholar 

  10. de Carvalho Niebel F, Frendo P, Van Montagu M, Cornelissen M: Post-transcriptional cosuppression of β-glucanase genes does not affect accumulation of transgene nuclear mRNA. Plant Cell 7: 347–358 (1995).

    Google Scholar 

  11. de Carvalho F, Gheysen G, Kushnir S, Van Montagu M, Inzé D, Castresana C: Suppression of β-1, 3-glucanase transgene expression in homozygous plants. EMBO J 11: 2595–2602 (1992).

    Google Scholar 

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

    Google Scholar 

  13. Elmayan T, Vaucheret H: Single copies of a 35S-driven transgene can undergo post-transcriptional silencing at each generation or can be transcriptionally inactivated in trans by a 35S silencer. Plant J 9: 787–797 (1996).

    Google Scholar 

  14. English JJ, Mueller E, Baulcombe DC: Suppression of virus accumulation in transgenic plants exhibiting silencing of nuclear genes. Plant Cell 8: 179–188 (1996).

    Google Scholar 

  15. Flavell RB, O'Dell M, Metzlaff M, Bonhomme S, and Cluster PD: Developmental regulation of co-suppression in Petunia hybrida. In: Meyer P (ed) Current Topics in Microbiology and Immunology Vol. 197: Gene Silencing in Higher Plants and Related Phenomena in Other Eukaryotes, Springer-Verlag, Berlin (1995).

    Google Scholar 

  16. Fray RG, Grierson D: Identification and genetic analysis of normal and mutant phytoene synthase genes of tomato by sequencing, complementation and co-suppression. Plant Mol Biol 22: 589–602 (1993).

    Google Scholar 

  17. Goodwin J, Chapman K, Parks TD, Wernsman EA, Dougherty WG: Genetic and biochemical dissection of transgenic RNA-mediated resistance. Plant Cell 8: 95–105 (1996).

    Google Scholar 

  18. Goring DR, Thomson L, Rothstein SJ: Transformation of a partial nopaline synthase gene in tobacco suppresses the expression of a resident wild-type gene. Proc Natl Acad Sci USA 88: 1770–1774 (1991).

    Google Scholar 

  19. Green PJ: Control of mRNA stability in higher plants. Plant Physiol 102: 1065–1070 (1993).

    Google Scholar 

  20. Grierson D, Fray RG, Hamilton AJ, Smith CJS, Watson CF: Does co-suppression of sense genes in transgenic plants involve antisense RNA? Trendo Biotechnol 9: 122–123 (1991).

    Google Scholar 

  21. Grierson D, Tucker GA, Keen J, Ray J, Bird CR, Schuch W: Sequencing and identification of a cDNA clone for tomato polygalacturonase. Nucl Acids Res 14: 8595–8603 (1986).

    Google Scholar 

  22. Hammond J, Kamo KK: Effective resistance to potyvirus infection conferred by expression of antisense RNA in transgenic plants. Mol Plant-Microbe Interact 8: 674–682 (1995).

    Google Scholar 

  23. Hart CM, Fischer B, Neuhaus JM, Meins FJr: Regulated inactivation of homologous gene-expression in transgenic nicotiana-sylvestris plants containing a defense-related tobacco chitinase gene. Mol Gen Genet 235: 179–188 (1992).

    Google Scholar 

  24. Hobbs SLA, Kpodar P, DeLong CMO: The effect of T-DNA copy number, position and methylation on reporter gene expression in tobacco transformants. Plant Mol Biol 15: 851–864 (1990).

    Google Scholar 

  25. Hobbs SLA, Warkentin TD, DeLong CMO: Transgene copy number can be positively or negatively associated with transgene expression. Plant Mol Biol 21: 17–26 (1993).

    Google Scholar 

  26. Ingelbrecht I, Van Houdt H, Van Montagu M, Depicker A: Posttranscriptional silencing of reporter transgenes in tobacco correlates with DNA methylation. Proc Natl Acad Sci USA 91: 10502–10506 (1994).

    Google Scholar 

  27. Jorgensen R, Que QD, English J, Cluster P, Napoli C: Sensesuppression of flower color genes as a sensitive reporter of epigenetic states of gene-expression in plant development. Plant Physiol 108: 14 (1995).

    Google Scholar 

  28. Jorgensen RA: Cosuppression, flower color patterns and metastable gene expression states. Science 268: 686–691 (1995).

    Google Scholar 

  29. Kawchuk LM, Martin RR, Mcpherson J: Sense and antisense RNA-mediated resistance to potato leafroll virus in Russet Burbank potato plants. Mol Plant-Microbe Interact 4: 247–253 (1991).

    Google Scholar 

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

    Google Scholar 

  31. Lindbo JA, Dougherty WG: Pathogen-derived resistance to a potyvirus: immune and resistant phenotypes in transgenic tobacco expressing altered forms of a potyvirus coat protein nucleotide sequence. Mol Plant-Microbe Interact 5: 144–153 (1992).

    Google Scholar 

  32. Lindbo JA, Dougherty WG: Untranslatable transcripts of the tobacco etch virus coat protein gene sequence can interfere with tobacco etch virus replication in transgenic plants and protoplasts. Virology 189: 725–733 (1992).

    Google Scholar 

  33. Lindbo JA, Silva-Rosales L, Proebsting WM, Dougherty WG: Induction of a highly specific antiviral state in transgenic plants: implications for regulation of gene expression and virus resistance. Plant Cell 5: 1749–1759 (1993).

    Google Scholar 

  34. Longstaff M, Brigneti G, Boccard F, Chapman S, Baulcombe DC: Extreme resistance to potato virus X infection in plants expressing a modified component of the putative viral replicase. EMBO J 12: 379–386 (1993).

    Google Scholar 

  35. Matzke MA, Matzke AJM: How and why do plants inactivate homologous (trans)genes? Plant Physiol 107: 6679–685 (1995).

    Google Scholar 

  36. Matzke MA, Matzke AJM, Sheid OM: Inactivation of repeated genes: DNA-DNA interaction? In: Paszkowski J (ed) Homologous Recombination and Gene Silencing in Plants. Kluwer Academic Publishers, Dordrecht (1995).

    Google Scholar 

  37. Matzke MA, Neuhuber F, Matzke AJM: A variety of epistatic interactions can occur between partially homologous transgene loci brought together by sexual crossing. Mol Gen Genet 236: 379–386 (1993).

    Google Scholar 

  38. Meyer P, Heidmann I: Epigenetic variants of a transgenic petunia line show hypermethylation in transgene DNA: an indication for specific recognition of foreign DNA in transgenic plants. Mol Gen Genet 243: 390–399 (1994).

    Google Scholar 

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

    Google Scholar 

  40. Mueller E, Gilbert JE, Davenport G, Brigneti G, Baulcombe DC. Homology-dependent resistance: transgenic virus resistance in plants related to homology-dependent gene silencing. Plant J 7: 1001–1013 (1995).

    Google Scholar 

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

    Google Scholar 

  42. Nellen W, Lichtenstein C: What makes an mRNA anti-senseitive? Trends Biochem Sci 18: 419–423 (1993).

    Google Scholar 

  43. Palmgren G, Mattson O, Okkels FT: Treatment of Agrobacterium or leaf disks with 5-azacytidine increases transgene expression in tobacco. Plant Mol Biol 21: 429–435 (1993).

    Google Scholar 

  44. Pang SZ, Slightom JL, Gonsalves D: Different mechanisms protect transgenic tobacco against tomato spotted wilt and impatiens necrotic spot tospoviruses. Bio/technology 11: 819–824 (1993).

    Google Scholar 

  45. Park Y-D, Papp I, Moscone EA, Iglesias VA, Vaucheret H, Matzke AJM, Matzke MA: 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 (1996).

    Google Scholar 

  46. Phillips RL, Matzke MA, Oono K: Treasure your exceptions. Plant Cell 7: 1522–1527 (1995).

    Google Scholar 

  47. Seymour GB, Fray RG, Hill P, Tucker GA: Down-regulation of two non-homologous endogenous tomato genes with a single chimaeric sense gene construct. Plant Mol Biol 23: 1–9 (1993).

    Google Scholar 

  48. Smith CJS, Watson CF, Bird CR, Ray J, Schuch W, Grierson D: Expression of a truncated tomato polygalacturonase gene inhibits expression of the endogenous gene in transgenic plants. Mol Gen Genet 224: 447–481 (1990).

    Google Scholar 

  49. Smith HA, Powers H, Swaney S, Brown C, Dougherty WG: Transgenic potato virus Y resistance in potato: evidence for an RNA-mediated cellular response. Phytopathology 85: 864–870 (1995).

    Google Scholar 

  50. Smith HA, Swaney SL, Parks TD, Wernsman EA, Dougherty WG: Transgenic plant virus resistance mediated by untranslatable sense RNAs: expression, regulation, and fate of nonessential RNAs. Plant Cell 6: 1441–1453 (1994).

    Google Scholar 

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

    Google Scholar 

  52. van der Krol AR, Mur LA, Beld M, Mol JNM, Stuitje AR: 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 (1990).

    Google Scholar 

  53. van der Vlugt RAA, Ruiter RK, Goldbach RW: evidence for sense RNA-mediated protection to PVYN in tobacco plants transformed with the viral coat protein cistron. Plant Mol Biol 20: 631–639 (1992).

    Google Scholar 

  54. Vaucheret H, Palauqui JC, Elmayan T, Moffatt B: Molecular and genetic analysis of nitrite reductase co-suppression in transgenic tobacco plants. Mol Gen Genet 248: 311–317 (1995).

    Google Scholar 

  55. Wagner EGH, Simons RW: Antisense RNA control in bacteria, phage and plasmids. Annu Rev Microbiol (1994).

  56. Wassenegger M, Heimes S, Riedel L, Sänger HL: Methylation of plant genome-integrated viroid cDNAs is induced upon replication of the corresponding viroid RNA: a novel mechanism of a RNA-directed sequence-specific de novo methylation of genes. Cell 76: 567–576 (1994).

    Google Scholar 

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  1. The Sainsbury Laboratory, John Innes Centre, NR4 7UH, Norwich, UK

    David C. Baulcombe

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Baulcombe, D.C. RNA as a target and an initiator of post-transcriptional gene silencing in trangenic plants. Plant Mol Biol 32, 79–88 (1996). https://doi.org/10.1007/BF00039378

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