Epigenetic silencing in transgenic plants

Epigenetic silencing is a natural phenomenon in which the expression of genes is regulated through modifications of DNA, RNA, or histone proteins. It is a mechanism for defending host genomes against the effects of transposable elements and viral infection, and acts as a modulator of expression of duplicated gene family members and as a silencer of transgenes. A major breakthrough in understanding the mechanism of epigenetic silencing was the discovery of silencing in transgenic tobacco plants due to the interaction between two homologous promoters. The molecular mechanism of epigenetic mechanism is highly complicated and it is not completely understood yet. Two different molecular routes have been proposed for this, that is, transcriptional gene silencing, which is associated with heavy methylation of promoter regions and blocks the transcription of transgenes, and post-transcriptional gene silencing (PTGS), the basic mechanism is degradation of the cytosolic mRNA of transgenes or endogenous genes. Undesired transgene silencing is of major concern in the transgenic technologies used in crop improvement. A complete understanding of this phenomenon will be very useful for transgenic applications, where silencing of specific genes is required. The current status of epigenetic silencing in transgenic technology is discussed and summarized in this mini-review.

[1]  A. Dietz-Pfeilstetter,et al.  Stability of transgene expression as a challenge for genetic engineering. , 2010 .

[2]  M. Van Montagu,et al.  Posttranscriptional silencing of reporter transgenes in tobacco correlates with DNA methylation. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[3]  H. Vaucheret,et al.  Systemic acquired silencing: transgene‐specific post‐transcriptional silencing is transmitted by grafting from silenced stocks to non‐silenced scions , 1997, The EMBO journal.

[4]  S. Naito,et al.  Post-transcriptional gene silencing in cultured rice cells. , 2000, Plant & cell physiology.

[5]  Peter Meyer,et al.  Transcriptional transgene silencing and chromatin components , 2000, Plant Molecular Biology.

[6]  H. Saedler,et al.  Endogenous and environmental factors influence 35S promoter methylation of a maize A1 gene construct in transgenic petunia and its colour phenotype , 1992, Molecular and General Genetics MGG.

[7]  F. Assaad,et al.  Epigenetic repeat-induced gene silencing (RIGS) inArabidopsis , 1993, Plant Molecular Biology.

[8]  C. Napoli,et al.  Introduction of a Chimeric Chalcone Synthase Gene into Petunia Results in Reversible Co-Suppression of Homologous Genes in trans. , 1990, The Plant cell.

[9]  B. Charrier,et al.  Co-silencing of homologous transgenes in tobacco , 2000, Molecular Breeding.

[10]  P. Waterhouse,et al.  A Branched Pathway for Transgene-Induced RNA Silencing in Plants , 2002, Current Biology.

[11]  Yun Jin,et al.  Transgene-induced gene silencing in plants. , 2015, Methods in molecular biology.

[12]  I. Baldwin,et al.  Progressive 35S promoter methylation increases rapidly during vegetative development in transgenic Nicotiana attenuata plants , 2013, BMC Plant Biology.

[13]  P. Meyer,et al.  Differences in DNA-methylation are associated with a paramutation phenomenon in transgenic petunia. , 1993, The Plant journal : for cell and molecular biology.

[14]  H. Vaucheret,et al.  A Transcriptionally Active State Is Required for Post-Transcriptional Silencing (Cosuppression) of Nitrate Reductase Host Genes and Transgenes. , 1997, The Plant cell.

[15]  H. Vaucheret,et al.  Post-transcriptional gene silencing in plants. , 2001, Journal of cell science.

[16]  Marjori Matzke,et al.  Targets of RNA-directed DNA methylation. , 2007, Current opinion in plant biology.

[17]  M. Pellegrini,et al.  Plants regenerated from tissue culture contain stable epigenome changes in rice , 2013, eLife.

[18]  Takahide Yokoi,et al.  Consistent transcriptional silencing of 35S-driven transgenes in gentian. , 2005, The Plant journal : for cell and molecular biology.

[19]  T. Mirkov,et al.  Posttranscriptional gene silencing in transgenic sugarcane. Dissection Of homology-dependent virus resistance in a monocot that has a complex polyploid genome , 1999, Plant physiology.

[20]  Waddington Ch,et al.  The epigenotype. 1942. , 2012 .

[21]  H. Saedler,et al.  HOMOLOGY-DEPENDENT GENE SILENCING IN PLANTS. , 1996, Annual review of plant physiology and plant molecular biology.

[22]  C D Day,et al.  Transgene integration into the same chromosome location can produce alleles that express at a predictable level, or alleles that are differentially silenced. , 2000, Genes & development.

[23]  D. Baulcombe,et al.  Retracted: Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana , 1998, The EMBO journal.

[24]  P. Waterhouse,et al.  Posttranscriptional gene silencing in plants. , 2004, Methods in molecular biology.

[25]  A. Hamilton,et al.  Potato Virus X Amplicons in Arabidopsis Mediate Genetic and Epigenetic Gene Silencing , 2000, Plant Cell.

[26]  T. Nakatsuka,et al.  De novo DNA methylation of the 35S enhancer revealed by high-resolution methylation analysis of an entire T-DNA segment in transgenic gentian , 2011 .

[27]  W. Dougherty,et al.  Transgenes and gene suppression: telling us something new? , 1995, Current opinion in cell biology.

[28]  G. Tucker,et al.  Inheritance and effect on ripening of antisense polygalacturonase genes in transgenic tomatoes , 1990, Plant Molecular Biology.

[29]  H. Vaucheret,et al.  (TRANS)GENE SILENCING IN PLANTS: How Many Mechanisms? , 2000, Annual review of plant physiology and plant molecular biology.

[30]  R. Twyman,et al.  Transgene Integration, Expression and Stability in Plants: Strategies for Improvements , 2010 .

[31]  M. Metzlaff,et al.  RNA-Mediated RNA Degradation and Chalcone Synthase A Silencing in Petunia , 1997, Cell.

[32]  R. Carthew,et al.  SnapShot: Posttranscriptional Gene Silencing , 2007, Cell.

[33]  A. Depicker,et al.  Epigenetic switches of tobacco transgenes associate with transient redistribution of histone marks in callus culture , 2013, Epigenetics.

[34]  H. Vaucheret,et al.  Frequencies, Timing, and Spatial Patterns of Co-Suppression of Nitrate Reductase and Nitrite Reductase in Transgenic Tobacco Plants , 1996, Plant physiology.

[35]  J. Mol,et al.  Flavonoid genes in petunia: addition of a limited number of gene copies may lead to a suppression of gene expression. , 1990, The Plant cell.

[36]  J. Kendall,et al.  The maize methylome influences mRNA splice sites and reveals widespread paramutation-like switches guided by small RNA , 2013, Genome research.

[37]  P. Meyer The role of chromatin remodeling in transgene silencing and plant development , 1999, In Vitro Cellular & Developmental Biology - Plant.

[38]  Potato Virus X , 1949, Nature.

[39]  E. Dennis,et al.  Transgene Expression and Transgene-Induced Silencing in Diploid and Autotetraploid Arabidopsis , 2011, Genetics.

[40]  Meeghan Sinclair,et al.  Transgene silencing , 2000, Nature Biotechnology.

[41]  Gerben Menschaert,et al.  Quality Evaluation of Methyl Binding Domain Based Kits for Enrichment DNA-Methylation Sequencing , 2013, PloS one.

[42]  H. L. Sänger,et al.  RNA-directed de novo methylation of genomic sequences in plants , 1994, Cell.

[43]  Helmut Gernsheim,et al.  W. H. Fox Talbot and the history of photography , 1977 .

[44]  J. J. English,et al.  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. , 1997, The Plant cell.

[45]  C. Dehio,et al.  Identification of plant genetic loci involved in a posttranscriptional mechanism for meiotically reversible transgene silencing. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[46]  R. Hellens,et al.  Epigenetic inactivation of chalcone synthase-A transgene transcription in petunia leads to a reversion of the post-transcriptional gene silencing phenotype. , 2007, Plant & cell physiology.

[47]  D. Inzé,et al.  Distinct phenotypes generated by overexpression and suppression of S-adenosyl-L-methionine synthetase reveal developmental patterns of gene silencing in tobacco. , 1994, The Plant cell.

[48]  A. Kohli,et al.  The Quest to Understand the Basis and Mechanisms that Control Expression of Introduced Transgenes in Crop Plants , 2006, Plant signaling & behavior.

[49]  P. Meyer,et al.  Condensation of chromatin in transcriptional regions of an inactivated plant transgene: evidence for an active role of transcription in gene silencing , 1997, Molecular and General Genetics MGG.

[50]  R. Twyman,et al.  Linear transgene constructs lacking vector backbone sequences generate low-copy-number transgenic plants with simple integration patterns , 2000, Transgenic Research.

[51]  H. Vaucheret,et al.  RDR2 Partially Antagonizes the Production of RDR6-Dependent siRNA in Sense Transgene-Mediated PTGS , 2012, PloS one.

[52]  K. Kalantidis,et al.  RNA silencing movement in plants , 2008, Biology of the cell.

[53]  D. Baulcombe,et al.  Retraction: ‘Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana’ , 2015, The EMBO journal.

[54]  M. Matzke,et al.  Transgene silencing by the host genome defense: implications for the evolution of epigenetic control mechanisms in plants and vertebrates , 2000, Plant Molecular Biology.

[55]  D. Somers,et al.  Transgenic DNA integrated into the oat genome is frequently interspersed by host DNA. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[56]  Donna M Bond,et al.  Epigenetic transitions leading to heritable, RNA-mediated de novo silencing in Arabidopsis thaliana , 2015, Proceedings of the National Academy of Sciences.

[57]  D. Baulcombe,et al.  Suppression of Virus Accumulation in Transgenic Plants Exhibiting Silencing of Nuclear Genes. , 1996, The Plant cell.

[58]  H. Vaucheret,et al.  Expression of single copies of a strongly expressed 35S transgene can be silenced post-transcriptionally , 1996 .

[59]  M. Montagu,et al.  Post-transcriptional gene silencing in plants. , 1997, Current opinion in cell biology.

[60]  S. Cutler,et al.  Sulfamethazine Suppresses Epigenetic Silencing in Arabidopsis by Impairing Folate Synthesis[W] , 2012, Plant Cell.

[61]  A. Carrá,et al.  Transgene silencing in grapevines transformed with GFLV resistance genes: analysis of variable expression of transgene, siRNAs production and cytosine methylation , 2010, Transgenic Research.

[62]  D. Baulcombe,et al.  Systemic Spread of Sequence-Specific Transgene RNA Degradation in Plants Is Initiated by Localized Introduction of Ectopic Promoterless DNA , 1998, Cell.

[63]  P. Meyer Epigenetic variation and environmental change. , 2015, Journal of experimental botany.

[64]  K. Folta,et al.  Transgene-induced silencing of Arabidopsis phytochrome A gene via exonic methylation. , 2007, The Plant journal : for cell and molecular biology.

[65]  S. Grewal,et al.  Heterochromatin: new possibilities for the inheritance of structure. , 2002, Current opinion in genetics & development.

[66]  N. L. Innes Global Status of Commercialized Biotech/GM Crops: 2005. ISAAA Briefs No. 34. By C. James. Ithaca, NY, USA: ISAAA (2005), pp. 46, US$50.00. ISBN 1-892456-38-9 , 2006, Experimental Agriculture.

[67]  M. Matzke,et al.  Endogenous targets of RNA‐directed DNA methylation and Pol IV in Arabidopsis , 2006, The EMBO journal.

[68]  P. Meyer,et al.  Epigenetic variants of a transgenic petunia line show hypermethylation in transgene DNA: an indication for specific recognition of foreign DNA in transgenic plants , 1994, Molecular and General Genetics MGG.

[69]  K. Shimamoto,et al.  De novo DNA methylation induced by siRNA targeted to endogenous transcribed sequences is gene-specific and OsMet1-independent in rice. , 2008, The Plant journal : for cell and molecular biology.

[70]  P. Meyer,et al.  Evidence for cytosine methylation of non‐symmetrical sequences in transgenic Petunia hybrida. , 1994, The EMBO journal.

[71]  V. Chandler,et al.  Transcriptionally Silenced Transgenes in Maize Are Activated by Three Mutations Defective in Paramutation , 2006, Genetics.

[72]  T. Eulgem,et al.  An alternative polyadenylation mechanism coopted to the Arabidopsis RPP7 gene through intronic retrotransposon domestication , 2013, Proceedings of the National Academy of Sciences.

[73]  M. Van Montagu,et al.  Silencing of beta-1,3-glucanase genes in tobacco correlates with an increased abundance of RNA degradation intermediates. , 1998, Nucleic acids research.

[74]  David C. Baulcombe,et al.  RNA as a target and an initiator of post-transcriptional gene silencing in trangenic plants , 1996, Plant Molecular Biology.

[75]  T. Hall,et al.  Recurrent onset of epigenetic silencing in rice harboring a multi-copy transgene. , 1998, The Plant journal : for cell and molecular biology.

[76]  K. Kasschau,et al.  A Counterdefensive Strategy of Plant Viruses Suppression of Posttranscriptional Gene Silencing , 1998, Cell.

[77]  A. Shrawat,et al.  Agrobacterium tumefaciens-mediated genetic transformation of barley (Hordeum vulgare L.) , 2007 .

[78]  S. Yadav,et al.  AtROS1 overexpression provides evidence for epigenetic regulation of genes encoding enzymes of flavonoid biosynthesis and antioxidant pathways during salt stress in transgenic tobacco , 2015, Journal of experimental botany.

[79]  K. Křížová,et al.  Gene Silencing , 2004 .

[80]  Eunseog Youn,et al.  Transgene Silencing and Transgene-Derived siRNA Production in Tobacco Plants Homozygous for an Introduced AtMYB90 Construct , 2012, PloS one.

[81]  Y. Helariutta,et al.  Transgene inactivation inPetunia hybrida is influenced by the properties of the foreign gene , 1995, Molecular and General Genetics MGG.

[82]  P. Ahmad,et al.  Role of transgenic plants in agriculture and biopharming. , 2012, Biotechnology advances.

[83]  H. Vaucheret,et al.  Transcriptional gene silencing in plants: targets, inducers and regulators. , 2001, Trends in genetics : TIG.

[84]  M. Primig,et al.  Reversible methylation and inactivation of marker genes in sequentially transformed tobacco plants , 1989, The EMBO journal.