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Mosaic patterns of transgene expression in plants

Russian Journal of Genetics volume 48, pages 249–260 (2012)Cite this article

Abstract

The review describes the phenomenon of mosaic transgene (gene) expression in plants. Parallels with the mosaic transgene (gene) expression in other organisms are presented. Parallels with the mosaic patterns of gene (transgene) expression in other organisms (Drosophila, transgenic animals, and others) are made.

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References

  1. Matzke, M., Primig, M., Trnovsky, J., and Matzke, A., Reversible Methylation and Inactivation of Marker Genes in Sequentially Transformed Plants, EMBO J., 1989, vol. 8, pp. 643–649.

    PubMed  CAS  Google Scholar 

  2. Napoli, C., Lemieux, C., and Jorgensen, R., Introduction of a Chimeric Chalcone Synthase Gene into Petunia Results in Reversible Co-Suppression of Homologous Genes in Trans, Plant Cell, 1990, vol. 2, pp. 279–289.

    PubMed  Article  CAS  Google Scholar 

  3. van der Krol, A.R., Mur, L.A., Beld, M., et al., Flavonoid Genes in Petunia: Addition of a Limited Number of Gene Copies May Lead to a Suppression of Gene Expression, Plant Cell, 1990, vol. 2, pp. 291–299.

    PubMed  Article  Google Scholar 

  4. Dorokhov, Yu.L., Gene Silencing in Plants, Mol. Biol., 2007, vol. 41, no. 4, pp. 579–592.

    Article  Google Scholar 

  5. Marenkova, T.V. and Deineko, E.V., Transcriptional Gene Silencing in Plants, Russ. J. Genet., 2010, vol. 46, no. 5, pp. 511–520.

    Article  CAS  Google Scholar 

  6. Flavell, R.B., Inactivation of Gene Expression in Plants as a Consequence of Specific Sequence Duplication, Proc. Natl. Acad. Sci. USA, 1994, vol. 91, pp. 3490–3496.

    PubMed  Article  CAS  Google Scholar 

  7. Matzke, M., Kanno, T., Daxinger, L., et al., RNA-Mediated Chromatin-Based Silencing in Plants, Curr. Opin. Cell Biol., 2009, vol. 21, pp. 367–376.

    PubMed  Article  CAS  Google Scholar 

  8. Chinnusamy, V. and Zhu, J.K., RNA-Directed DNA Methylation and Demethylation in Plants, Sci. China C Life Sci., 2009, vol. 52, pp. 331–343.

    PubMed  Article  CAS  Google Scholar 

  9. Wierzbicki, A., Haag, J.R., and Pikaard, C.S., Noncoding Transcription by RNA Polymerase Pol IVb/Pol V Mediates Transcriptional Silencing of Overlapping and Adjacent Genes, Cell, 2008, vol. 135, pp. 635–648.

    PubMed  Article  CAS  Google Scholar 

  10. Pikaard, C.S., Haag, J.R., Ream, T., and Wierzbicki, A.T., Roles of RNA Polymerase IV in Gene Silencing, Trends Plant Sci., 2008, vol. 13, pp. 390–397.

    PubMed  Article  CAS  Google Scholar 

  11. Li, C.F., Henderson, I.R., Song, L., et al., Dynamic Regulation of ARGONAUTE4 within Multiple Nuclear Bodies in Arabidopsis thaliana, PLoS Genet., 2008, vol. 4. e27.

    Google Scholar 

  12. Jinek, M. and Doudna, J.A., A Three-Dimensional View of the Molecular Machinery of RNA Interference, Nature, 2009, vol. 457, pp. 405–412.

    PubMed  Article  CAS  Google Scholar 

  13. Eamens, A., Wang, M.B., Smith, N.A., and Waterhouse, P.M., RNA Silencing in Plants: Yesterday, Today, and Tomorrow, Plant Physiol., 2008, vol. 147, pp. 456–468.

    PubMed  Article  CAS  Google Scholar 

  14. Vaucheret, H., Post-Transcriptional Small RNA Pathways in Plants: Mechanisms and Regulations, Genes Dev., 2006, vol. 20, pp. 759–771.

    PubMed  Article  CAS  Google Scholar 

  15. Dolgosheina, E.V., Morin, R.D., Aksay, G., et al., Conifers Have a Unique Small RNA Silencing Signature, RNA, 2008, vol. 14, pp. 1508–1515.

    PubMed  Article  CAS  Google Scholar 

  16. Marenkova (Novoselia), T.V., Deineko, E.V., and Shumny, V.K., Mosaic Expression Pattern of the nptII Gene in Transgenic Tobacco Plants Nu 21, Russ. J. Genet., 2007, vol. 43, no. 7, pp. 780–790.

    Article  CAS  Google Scholar 

  17. Morino, K., Olsen, O.A., and Shimamoto, K., Silencing of an Aleurone-Specific Gene in Transgenic Rice Is Caused by a Rearranged Transgene, Plant J., 1999, vol. 17, pp. 275–285.

    PubMed  Article  CAS  Google Scholar 

  18. Day, C.D., Lee, E., Kobayashi, J., et al., Transgene Integration into the Same Chromosome Location Can Produce Alleles That Express at a Predictable Level, or Alleles That Are Differentially Silenced, Genes Dev., 2000, vol. 14, pp. 2869–2880.

    PubMed  Article  CAS  Google Scholar 

  19. Bastar, M.T., Luthar, Z., Skof, S., and Bohanec, B., Quantitative Determination of Mosaic GFP Gene Expression in Tobacco, Plant Cell Rep., 2004, vol. 22, pp. 939–944.

    PubMed  Article  CAS  Google Scholar 

  20. Linn, F., Heidmann, I., Saedler, H., and Meyer, P., Epigenetic Changes in the Expression of the Maize A1 Gene in Petunia hybrida: Role of Numbers of Integrated Copies and State of Methylation, Mol. Gen. Genet., 1990, vol. 222, pp. 329–336.

    PubMed  Article  CAS  Google Scholar 

  21. Schmulling, T. and Rohrig, H., Gene Silencing in Transgenic Tobacco Hybrids: Frequency of the Event and Visualization of Somatic Inactivation Pattern, Mol. Gen. Genet., 1995, vol. 249, pp. 375–390.

    PubMed  Article  CAS  Google Scholar 

  22. Mannerlof, M. and Tenning, P., Variability of Gene Expression in Transgenic Tobacco, Euphytica, 1997, vol. 98, pp. 133–139.

    Article  Google Scholar 

  23. Pret`ova, A., Obert, B., and Wetzstein, H.Y., Leaf Developmental Stage and Tissue Location Affect the Detection of β-Glucuronidase in Transgenic Tobacco Plants, Biotechnol. Lett., 2001, vol. 23, pp. 555–558.

    Article  CAS  Google Scholar 

  24. Halfhill, M.D., Millwood, R.J., Rufty, T.W., et al., Spatial and Temporal Patterns of Green Fluorescent Protein (GFP) Fluorescence during Leaf Development in Transgenic Oilseed Rape, Brassica napus L., Plant Cell Rep., 2003, vol. 22, pp. 338–343.

    Article  CAS  Google Scholar 

  25. Koes, R.E., Spelt, C.E., Elzen, P.J.M., and Mol, J.N.M., Cloning and Molecular Characterization of the Chalcone Synthase Multigene Family of Petunia hybrid, Gene, 1989, vol. 81, pp. 245–257.

    PubMed  Article  CAS  Google Scholar 

  26. De Paoli, E., Accerbi, M., Jeong, D.H., et al., Distinct Extremely Abundant siRNAs Associated with Cosuppression in Petunia, RNA, 2009, vol. 15, pp. 1965–1970.

    PubMed  Article  Google Scholar 

  27. Davies, G.J., Sheikh, M.A., Ratcliffe, O.J., et al., Genetics of Homology-Dependent Gene Silencing in Arabidopsis: A Role for Methylation, Plant J., 1997, vol. 12, pp. 791–804.

    PubMed  Article  CAS  Google Scholar 

  28. Meyer, P. and 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., 1994, vol. 243, pp. 390–399.

    PubMed  CAS  Google Scholar 

  29. Matzke, M.A. and Matzke, A.J.M., Differential Inactivation and Methylation of a Transgene in Plants by Two Suppressor Loci Containing Homologous Sequences, Plant. Mol. Biol., 1991, vol. 16, pp. 821–830.

    PubMed  Article  CAS  Google Scholar 

  30. Matzke, A.J.M., Neuhuber, F., Park, Y.-D., et al., Homology-Dependent Gene Silencing in Transgenic Plants: Epistatic Silencing Loci Contain Multiple Copies of Methylated Transgenes, Mol. Gen. Genet., 1994, vol. 244, pp. 219–229.

    PubMed  Article  CAS  Google Scholar 

  31. Neuhuber, F., Park, Y-D., Matzke, A.J.M., and Matzke, M.A., Susceptibility of Transgene Loci to Homology-Dependent Gene Silencing, Mol. Gen. Genet., 1994, vol. 244, pp. 230–241.

    PubMed  Article  CAS  Google Scholar 

  32. Iglesias, V.A., Moscone, E.A., Papp, I., et al., Molecular and Cytogenetic Analyses of Stably and Unstably Expressed Transgene Loci in Tobacco, Plant Cell, 1997, vol. 9, pp. 1251–1264.

    PubMed  Article  CAS  Google Scholar 

  33. Kilby, N.J., Leyser, H.M.O., and Furner, I.J., Promoter Methylation and Progressive Transgene Inactivation in Arabidopsis, Plant. Mol. Biol., 1992, vol. 20, pp. 103–112.

    PubMed  Article  CAS  Google Scholar 

  34. Meza, T., Kamfjord, D., Hakelien, A.-M., et al., The Frequency of Silencing in Arabidopsis thaliana Varies Highly between Progeny of Siblings and Can Be Influenced by Environmental Factors, Transgenic Res., 2001, vol. 10, pp. 63–67.

    Article  Google Scholar 

  35. Loginova, D.B., Shumnyi, V.K., and Deineko, E.V., Features of T-DNA Insert Organization in Transgenic Tobacco-Plants, Line Nu 21, Vest. VOGiS, 2010, vol. 14, no. 1, pp. 659–665.

    Google Scholar 

  36. Charrier, B., Scollan, C., Ross, S., et al., Co-Silencing of Homologous Transgenes in Tobacco, Mol. Breed., 2000, vol. 6, pp. 407–419.

    Article  CAS  Google Scholar 

  37. Meyer, P., Heidmann, I., and Niedenhof, I., Differences in DNA-Methylation Are Associated with a Paramutation Phenomenon in Transgenic Petunia, Plant J., 1993, vol. 4, pp. 89–100.

    PubMed  Article  CAS  Google Scholar 

  38. Ten Lohuis, M., Muller, A., Heidmann, I., et al., A Repetitive DNA Fragment Carrying a Hot Spot for de novo DNA Methylation Enhances Expression Variegation in Tobacco and Petunia, Plant J., 1995, vol. 8, pp. 919–932.

    PubMed  Article  CAS  Google Scholar 

  39. Mueller, A., Marins, M., Kamisugi, Y., and Meyer, P., Analysis of Hypermethylation in the RPS Element Suggests a Signal Function for Short Inverted Repeats in de novo Methylation, Plant. Mol. Biol., 2002, vol. 48, pp. 383–399.

    Article  Google Scholar 

  40. Kunz, C., Narangajavana, J., Jakowitsch, J., et al., Studies on the Effects of a Flanking Repetitive Sequence on the Expression of Single-Copy Trans-genes in Nicotiana sylvestris and in N. sylvestris-N. tomentosiformis Hybrids, Plant. Mol. Biol., 2003, vol. 52, pp. 203–215.

    PubMed  Article  CAS  Google Scholar 

  41. Takeda, S., Tadele, Z., Hofmann, I., et al., BRU1, a Novel Link between Responses to DNA Damage and Epigenetic Gene Silencing in Arabidopsis, Genes Dev., 2004, vol. 18, pp. 782–793.

    PubMed  Article  CAS  Google Scholar 

  42. Ono, T., Kaya, H., Takeda, S., et al., Chromatin Assembly Factor 1 Ensures the Stable Maintenance of Silent Chromatin States in Arabidopsis, Genes Cells, 2006, vol. 11, pp. 153–162.

    PubMed  Article  CAS  Google Scholar 

  43. Meyer, P., Linn, F., Heidmann, I., et al., Endogenous and Environmental Factors Influence 35S Promoter Methylation of a Maize A1 Gene Construct in Trans-genic Petunia and Its Color Phenotype, Mol. Gen. Genet., 1992, vol. 231, pp. 345–352.

    PubMed  Article  CAS  Google Scholar 

  44. Jorgensen, R., Developmental Significance of Epigenetic Impositions on the Plant Genome: A Paragenetic Function for Chromosomes, Dev. Genet., 1994, vol. 15, pp. 523–532.

    Article  Google Scholar 

  45. Robbins, M.L., Wang, P., Sekhon, R.S., and Chopra, S., Gene Structure Induced Epigenetic Modifications of pericarp color1 Alleles of Maize Result in Tissue-Specific Mosaicism, PLoS ONE, 2009, vol. 4, no. 12, pp. 1–12.

    Article  Google Scholar 

  46. Walker, E.L., Paramutation of the r1 Locus of Maize Is Associated with Increased Cytosine Methylation, Genetics, 1998, vol. 148, pp. 1973–1981.

    PubMed  CAS  Google Scholar 

  47. Suter, C.M. and Martin, I.K., Paramutation: The Tip of an Epigenetic Iceberg?, Trends Genet., 2009, vol. 26, no. 1, pp. 9–14.

    PubMed  Article  Google Scholar 

  48. Ehlert, B., Schottler, M.A., Tischendorf, G., et al., The Paramutated SULFUREA Locus of Tomato Is Involved in Auxin Biosynthesis, J. Exp. Bot., 2008, vol. 59, no. 13, pp. 3635–3647.

    PubMed  Article  CAS  Google Scholar 

  49. Bollmann, J., Carpenter, R., and Coen, E.S., Allelic Interactions at the nivea Locus of Antirrhinum, Plant Cell, 1991, vol. 3, pp. 1327–1336.

    PubMed  Article  CAS  Google Scholar 

  50. Chandler, V.L., Paramutation: From Maize to Mice, Cell, 2007, vol. 128, pp. 641–645.

    PubMed  Article  CAS  Google Scholar 

  51. Stam, M., Paramutation: A Heritable Change in Gene Expression by Allelic Interactions in Trans, Mol. Plant, 2009, vol. 2, no. 4, pp. 578–588.

    PubMed  Article  CAS  Google Scholar 

  52. Koryakov, D.E. and Zhimulev, I.F., Khromosomy: Struktura i funktsii (Chromosomes: Structure and Functions), Novosibirsk: Izd. Sib. Otd. Ross. Akad. Nauk, 2009.

    Google Scholar 

  53. Ebbs, M.L., Bartee, L., and Bender, J., H3 Lysine 9 Methylation Is Maintained on a Transcribed Inverted Repeat by Combined Action of SUVH6 and SUVH4 Methyltransferases, Mol. Cell Biol., 2005, vol. 25, pp. 10507–10515.

    PubMed  Article  CAS  Google Scholar 

  54. Verdel, A. and Moazed, D., RNAi-Directed Assembly of Heterochromatin in Fission Yeast, FEBS Lett., 2005, vol. 579, pp. 5872–5878.

    PubMed  Article  CAS  Google Scholar 

  55. Ayoub, N., Goldshmidt, I., and Cohen, A., Position Effect Variegation at the Mating-Type Locus of Fission Yeast: A Cis-Acting Element Inhibits Covariegated Expression of Genes in the Silent and Expressed Domains, Genetics, 1999, vol. 152, pp. 495–508.

    PubMed  CAS  Google Scholar 

  56. Serova, I.A., Andreeva, L.E., Khaidarova, N.V., et al., Mosaic Expression of the lacZ Reporter-Gene under Control of 5′-Regulatory Sequencies of the Alpha-S1-Casein Gene in Transgenic Mice, Tsitologiya, 2009, vol. 51, no. 11, pp. 917–923.

    CAS  Google Scholar 

  57. Wang, Y., Flemming, B.P., Martin, C.C., et al., Long-Range Enhancers Are Required to Maintain Expression of the Autoantigen Islet-Specific Glucose-6-Phosphatase Catalytic Subunit-Related Protein in Adult Mouse Islets in vivo, Diabetes, 2008, vol. 57, pp. 133–141.

    PubMed  Article  CAS  Google Scholar 

  58. Bismuth, K., Skuntz, S., and Hallsson, J.H., An Unstable Targeted Allele of the Mouse Mitf Gene with a High Somatic and Germline Reversion Rate, Genetics, 2008, vol. 178, pp. 259–272.

    PubMed  Article  CAS  Google Scholar 

  59. Festenstein, R., Tolaini, M., Corbella, P., et al., Locus Control Region Function and Heterochromatin-Induced Position Effect Variegation, Science, 1996, vol. 271, pp. 1123–1125.

    PubMed  Article  CAS  Google Scholar 

  60. Milot, E., Strouboulis, J., Trimborn, T., et al., Hetero-chromatin Effects on the Frequency and Duration of LCR-Mediated Gene Transcription, Cell, 1996, vol. 87, pp. 105–114.

    PubMed  Article  CAS  Google Scholar 

  61. Saveliev, A., Everett, C., Sharpe, T., et al., DNA Triplet Repeats Mediate Heterochromatin-Protein-1-Sensitive Variegated Gene Silencing, Nature, 2003, vol. 422, pp. 909–913.

    PubMed  Article  CAS  Google Scholar 

  62. Krepulat, F., Lohler, J., Heinlein, C., et al., Epigenetic Mechanisms Affect Mutant p53 Transgene Expression in WAP-mutp53 Transgenic Mice, Oncogene, 2005, vol. 24, pp. 4645–4659.

    PubMed  Article  CAS  Google Scholar 

  63. Liew, C.G., Draper, J.S., Walsh, J., et al., Transient and Stable Transgene Expression in Human Embryonic Stem Cells, Stem Cells, 2007, vol. 25, pp. 1521–1528.

    PubMed  Article  CAS  Google Scholar 

  64. Yamasaki, T., Miyasaka, H., and Ohama, T., Unstable RNAi Effects through Epigenetic Silencing of an Inverted Repeat in Chlamydomonas reinhardtii, Genetics, 2008, vol. 180, pp. 1927–1944.

    PubMed  Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Institute of Cytology and Genetics, Siberian Branch, Russian Academy of Sciences, Novosibirsk, 630090, Russia

    T. V. Marenkova, D. B. Loginova & E. V. Deineko

Authors
  1. T. V. Marenkova
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  2. D. B. Loginova
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  3. E. V. Deineko
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Correspondence to E. V. Deineko.

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Original Russian Text © T.V. Marenkova, D.B. Loginova, E.V. Deineko, 2012, published in Genetika, 2012, Vol. 48, No. 3, pp. 293–306.

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Marenkova, T.V., Loginova, D.B. & Deineko, E.V. Mosaic patterns of transgene expression in plants. Russ J Genet 48, 249–260 (2012). https://doi.org/10.1134/S1022795412030088

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  • DOI: https://doi.org/10.1134/S1022795412030088

Keywords

  • Transgenic Plant
  • Transcriptional Silence
  • Mosaic Pattern
  • uidA Gene
  • Heterochromatin Region