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Target sites for SINE integration in Brassica genomes display nuclear matrix binding activity

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Abstract

Short interspersed nuclear elements (SINEs) are ubiquitous components of complex animal and plant genomes. SINEs are believed to be important players in eukaryotic genome evolution. Studies on SINE integration sites have revealed non-random integration without strict nucleotide sequence requirements for the integration target, suggesting that the targeted DNA might assume specific secondary structures or protein associations. Here, we report that S1 SINE elements in the genomes of Brassica show an interesting preference for matrix attachment regions (MARs). Ten cloned genomic regions were tested for their ability to bind the nuclear matrix both before and after a SINE integration event. Eight of the genomic regions targeted by S1 display strong affinity for the nuclear matrix, while two show weaker binding. The SINE S1 did not display any matrix-binding capacity on its own in either non-methylated or methylated forms. In vivo, an integrated S1 is methylated while the surrounding genomic regions may remain undermethylated or undergo methylation. However, tested genomic regions containing methylated'S1, with or without methylated flanking genomic sequences, were found to vary in their ability to bind the matrix in vitro. These results suggest a possible molecular basis for a preferential targeting of SINEs to MARs and a possible impact of the integration events upon gene and genome function.

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References

  • Allen G, Hall G Jr, Michalowski S et al. (1996) High-level transgene expression in plant cells: effects of a strong scaffold attachment region from tobacco. Plant Cell 8: 899–913.

    Article  PubMed  CAS  Google Scholar 

  • Arnaud P, Goubely C, Deragon JM (2000) SINE retroposons can be used in-vivo as nucleation centers for de novo methylation. Mol Cell Biol 20: 3434–3441.

    Article  PubMed  CAS  Google Scholar 

  • Avramova Z, Bennetzen JL (1993) Isolation of nuclear matrices from maize leaves; Identification of a matrix binding site adjacent to the maize Adh1 gene. Plant Mol Biol 22: 1135–1143.

    Article  PubMed  CAS  Google Scholar 

  • Avramova Z, SanMiguel P, Georgieva E, Bennetzen JL (1995) Matrix attachment regions and transcribed sequences within a long chromosomal continuum containing maize adh1. Plant Cell 7: 1667–1680.

    Article  PubMed  CAS  Google Scholar 

  • Avramova Z, Tikhonov A, Chen M, Bennetzen JL (1998) Matrix-attachment regions in colinear segments of the sorghum and rice genomes. Nucleic Acids Res 26: 761–767.

    Article  PubMed  CAS  Google Scholar 

  • Benham C, Kohwi-Shigematsu T, Bode J (1997) Stress-induced duplex DNA destabilization in scaffold/matrix attachment regions. J Mol Biol 274: 181–196.

    Article  PubMed  CAS  Google Scholar 

  • Bode J, Kohwi Y, Dickinson L et al. (1992) Biological signifi-cance of unwinding capability of nuclear matrix associating DNAs. Science 255: 195–197.

    PubMed  CAS  Google Scholar 

  • Bode J, Bartsch J, Mielke C, Schubler D, Seibler J, Benham C, Boulikas T, Iber MC (1998) Transcription-promoting genomic sites in mammalia: their elucidation and architec-tural principles. Gene Therapy Mol Biol 1: 551–580.

    Google Scholar 

  • Breyne P, van Montague M, Depicker A, Gheysen G (1992) Characterization of a plant scaffold-attachment region in DNA fragment that normalizes transgene expression in tobacco. Plant Cell 4: 463–471.

    Article  PubMed  CAS  Google Scholar 

  • Bruni R, Argentini C, D'Ugo E, Ciccaglione A, Rapicetta M (1995) Recurrence of WHV integration in the b3n locus in woodchuck hepatocellular carcinoma. Virology 214: 229–234.

    Article  PubMed  CAS  Google Scholar 

  • Capy P, Bazin C, Higuet D, Langin T (1998) Dynamics and Evolution of Transposable Elements. Austin Texas, USA: RG Landes Company, Springer, pp 37–47.

    Google Scholar 

  • Chinn AM, Comai L (1996) The heat shock cognate 80 gene of tomato is £anked by matrix attachment regions. Plant Mol Biol 32: 959–968.

    Article  PubMed  CAS  Google Scholar 

  • Cockerill PN, Garrard WT (1986a) Chromosomal loop anchor-age sites appear to be evolutionarily conserved. FEBS Lett 204: 5–7.

    Article  PubMed  CAS  Google Scholar 

  • Cockerill PN, Garrard WT (1986b) Chromosomal loop anchor-age of the kappa immunoglobulin gene occurs next to the enhancer in a region containing topoisomerase II sites. Cell 44: 273–282.

    Article  PubMed  CAS  Google Scholar 

  • Cost GJ, Boeke JD (1998) Targeting of human retroposon inte-gration is directed by the specificity of the L1 endonuclease for regions of unusual DNA structure. Biochemistry 37: 18081–18093.

    Article  PubMed  CAS  Google Scholar 

  • Craig NL (1997) Target site selection in transposition. Annu Rev Biochem 66: 437–474.

    Article  PubMed  CAS  Google Scholar 

  • Deragon JM, Landry BS, Pelisser T, Tutois S, Picard G (1994) Analysis of retroposition in plants based on a family of SINEs from Brassica napus. J Mol Evol 39: 378–386.

    Article  PubMed  CAS  Google Scholar 

  • Deragon JM, Gilbert N, Rouquet L, Lenoir A, Arnaud P, Picard G (1996) A transcriptional analysis of the S1Bn (Brassica napus) family of SINE retroposons. Plant Mol Biol 32: 869–878.

    Article  PubMed  CAS  Google Scholar 

  • Dietz A, Kay V, Schlake T, Landsmann J, Bode J (1994) A plant scaffold attached region detected close to a T-DNA integration site is active in mammalian cells. Nucleic Acids Res 22: 2744–2751.

    PubMed  CAS  Google Scholar 

  • Doolittle WF, Sapienza C (1980) Selfish genes, the phenotype paradigm and genome evolution. Nature 284: 601–603.

    Article  PubMed  CAS  Google Scholar 

  • Evans IM, Gatehouse LN, Gatehouse JA, Yarwood JN, Boulter D, Croy RRD (1990) The extensin gene family in oilseed rape (Brassica napus L.): characterization of sequences of representative members of the family. Mol Gen Genet 223: 273–287.

    PubMed  CAS  Google Scholar 

  • Flavell RB, Bennet MD, Smith JB, Smith DB (1974) Genome size and the proportion of repeated nucleotide sequence DNA in plants. Biochem Genet 12: 257–269.

    Article  PubMed  CAS  Google Scholar 

  • Goubely C, Arnaud P, Tatout C, Heslop-Harrison JS, Deragon JM(1999) S1 SINE retroposons are methylated at symmetri-cal and non-symmetrical positions in Brassica napus: Identi-fication of a preferred target site for asymmetrical methylation. Plant Mol Biol 39: 243–255.

    Article  PubMed  CAS  Google Scholar 

  • Grandbastien MA (1992) Retroelements in higher plants. Trends Genet 8: 103–108.

    PubMed  CAS  Google Scholar 

  • Hellmann-Blumberg U, McCarthy-Hintz MF, Gatewood JM, Schmid CW (1993) Developmental differences in methyl-ation of human Alu repeats. Mol Cell Biol 13: 4523–4530.

    PubMed  CAS  Google Scholar 

  • Hibino Y, Ohzeki H, Hirose N, Morita Y, Sugano N (1998) Involvement of DNA methylation in binding a highly repeti-tive DNA component to nuclear scaffold proteins from rat liver. Biochem Biophys Res Commun 252: 296–301.

    Article  PubMed  CAS  Google Scholar 

  • Holmes-Davis R, Comai, L (1998) Nuclear matrix attachment regions and plant gene expression. Trends Plant Sci 3: 91–97.

    Article  Google Scholar 

  • Homberger HP (1989) Bent DNA is a structural feature of scaffold-attached regions in Drosophila interphase nuclei. Chromosoma 98: 99–104.

    Article  PubMed  CAS  Google Scholar 

  • Iglesias V, Moscone E, Papp I et al. (1997) Molecular and cytogenetic analysis of stably and unstably expressed transgene loci in tobacco. Plant Cell 9: 1251–1264.

    Article  PubMed  CAS  Google Scholar 

  • Jurka J (1997) Sequence patterns indicate an enzymatic involve-ment in integration of mammalian retroposons. Proc Natl AcadSci USA 94: 1872–1877.

    Article  CAS  Google Scholar 

  • Jurka J, Klonowski P, Trifonov E (1998) Mammalian retroposons integrate at kinkable DNA sites. J Biomol Struct Dynamics 15: 717–721.

    CAS  Google Scholar 

  • Kidwell M, Lisch D (1997) Transposable elements as sources of variation in animals and plants. Proc Natl Acad Sci USA 94: 7704–7711.

    Article  PubMed  CAS  Google Scholar 

  • Kochanek S, Renz D, Doer£er W (1993) DNA methylation in the Alu sequences of diploid and haploid primary human cells. EMBO J 12: 1141–1151.

    PubMed  CAS  Google Scholar 

  • Kohwi-Shigematsu T, Kohwi Y (1997) High unwinding capa-bility of matrix attachment regions and ATC-sequence con-text-specific MAR-binding proteins. In: Berezney, R and Stein, G, eds. Nuclear Structure and Gene Expression, New York: Academic Press, pp 111–114.

    Google Scholar 

  • Labuda D, Zietkiewick E, Mitchell GA (1995) Alu elements as a source of genomic variation: deleterious effects and evol-utionary novelties. In: Maraia RJ ed. The Impact of Short Interspersed Elements (SINEs) on theHost Genome, Austin, Texas, USA: RG Landes Company, Springer, pp 1–24.

    Google Scholar 

  • Lapitan NL (1992) Organization and evolution of higher plant nuclear genomes. Genome 35: 171–181.

    CAS  Google Scholar 

  • Laurie DA, Bennett MD (1985) Nuclear DNA content in the genra Zea and Sorghum. Intergenic, interspecific and intraspecific variation. Heredity 55: 307–313.

    Google Scholar 

  • Lenoir A, Cournoyer B, Warwick SI, Picard G, Deragon JM (1997) Evolution of SINE S1 retrotransposons in Cruciferae plant species. Mol Biol Evol 14: 934–941.

    PubMed  CAS  Google Scholar 

  • Muller HP, Varmus HE (1994) DNA bending creates favored sites for retroviral integration: an explanation for preferred insertion sites in nucleosomes. EMBO J 13: 4704–4714.

    PubMed  CAS  Google Scholar 

  • Orgel LE, Crick FH (1980) Selfish DNA: the ultimate parasite. Nature 284: 604–607.

    Article  PubMed  CAS  Google Scholar 

  • Romig H, Ruff J, Fackelmeyer F, Patil M, Richter A (1994) Characterization of two intronic nuclear matrix attachment regions in the human DNA topoisomerase I gene. Eur J Biochem 221: 411–419.

    Article  PubMed  CAS  Google Scholar 

  • SanMiguel P, Bennetzen JL (1998) Evidence that recent increase in maize genome size was caused by the massive amplification of intergene retrotransposons. Annals Bot 82: 37–44.

    Article  CAS  Google Scholar 

  • SanMiguel P, Tikhonov A, Jin YK et al. (1996) Nested retrotransposons in the intergenic regions of the maize gen-ome. Science 274: 765–768.

    Article  PubMed  CAS  Google Scholar 

  • SanMiguel P, Gaut B, Tikhonov A, Nakajima Y, Bennetzen, JL (1998) The paleontology of intergene retrotransposons in maize. Nature Genet 20: 43–45.

    Article  PubMed  CAS  Google Scholar 

  • Sawasaki T, Takahashi M, Goshima N, Morikawa H (1998) Structures of transgene loci in transgenic Arabidopsis plants obtained by particle bombardment: junction regions can bind to nuclear matrices. Gene 218: 27–35.

    Article  PubMed  CAS  Google Scholar 

  • Stephanova E, Stancheva R, Avramova Z (1993) Binding of sequences from the 50 and 30–nontranscribed spacers of the rat rDNA locus to the nucleolar matrix. Chromosoma 102: 287–295.

    Article  PubMed  CAS  Google Scholar 

  • Tatout C, Lavie L, Deragon JM (1998) Similar target site selection occurs in integration of plant and mammalian retroposons. J Mol Evol 47: 463–470. 336 A. P. Tikhonov et al.

    Article  PubMed  CAS  Google Scholar 

  • Tatout C, Warwick SI, Lenoir A, Deragon JM (1999) SINE insertions as clade markers for wild crucifer species. Mol Biol Evol 16: 1614–1621.

    CAS  Google Scholar 

  • Tikhonov AP, SanMiguel PJ, Nakajima Y, Gorenstein N, Bennetzen JL, Avramova Z (1999) Colinearity and its excep-tions in orthologous adh regions of maize and sorghum. Proc Natl Acad Sci USA 96: 7409–7414.

    Article  PubMed  CAS  Google Scholar 

  • Tikhonov A, Bennetzen JL, Avramova Z (2000) Structural domains andMARs along large colinear adh regions ofmaize and sorghum. Plant Cell 12: 249–264.

    Article  PubMed  CAS  Google Scholar 

  • Ulker B, Allen GC, Thompson WF, Spiker S, Weissinger, AK (1999) A tobacco matrix attachment region reduces the loss of transgene expression in the progeny of transgenic tobacco plants. Plant J 18: 253–264.

    Article  CAS  Google Scholar 

  • van der Geest AHM, Hall GE, Spiker S, Hall TC (1994) The phaseolin gene is £anked by matrix-attachment regions. Plant J 6: 413–423.

    Article  CAS  Google Scholar 

  • van Drunen C, Oosterling R, Keultjes G, Weisbeek P, van Driel R, Smeekens CM (1997) Analysis of the chromatin domain organization around the plastocyanin gene reveals a MAR-specific sequence in Arabidopsis thaliana. Nucleic Acids Res 25: 3904–3911.

    Article  PubMed  CAS  Google Scholar 

  • Weitzel J, Buhrmester H, Straetling W (1997) Chicken MAR-binding protein ARBP is homologous to rat methyl-CpG-binding protein MeCP2. Mol Cell Biol 17: 5656–5666.

    PubMed  CAS  Google Scholar 

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Tikhonov, A.P., Lavie, L., Tatout, C. et al. Target sites for SINE integration in Brassica genomes display nuclear matrix binding activity. Chromosome Res 9, 325–337 (2001). https://doi.org/10.1023/A:1016650830798

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