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. 1997 Oct 1;25(19):3904–3911. doi: 10.1093/nar/25.19.3904

Analysis of the chromatin domain organisation around the plastocyanin gene reveals an MAR-specific sequence element in Arabidopsis thaliana.

C M van Drunen 1, R W Oosterling 1, G M Keultjes 1, P J Weisbeek 1, R van Driel 1, S C Smeekens 1
PMCID: PMC146963  PMID: 9380515

Abstract

The Arabidopsis thaliana genome is currently being sequenced, eventually leading towards the unravelling of all potential genes. We wanted to gain more insight into the way this genome might be organized at the ultrastructural level. To this extent we identified matrix attachment regions demarking potential chromatin domains, in a 16 kb region around the plastocyanin gene. The region was cloned and sequenced revealing six genes in addition to the plastocyanin gene. Using an heterologous in vitro nuclear matrix binding assay, to search for evolutionary conserved matrix attachment regions (MARs), we identified three such MARs. These three MARs divide the region into two small chromatin domains of 5 kb, each containing two genes. Comparison of the sequence of the three MARs revealed a degenerated 21 bp sequence that is shared between these MARs and that is not found elsewhere in the region. A similar sequence element is also present in four other MARs of Arabidopsis.Therefore, this sequence may constitute a landmark for the position of MARs in the genome of this plant. In a genomic sequence database of Arabidopsis the 21 bp element is found approximately once every 10 kb. The compactness of the Arabidopsis genome could account for the high incidence of MARs and MRSs we observed.

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Selected References

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  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  2. Amati B. B., Gasser S. M. Chromosomal ARS and CEN elements bind specifically to the yeast nuclear scaffold. Cell. 1988 Sep 23;54(7):967–978. doi: 10.1016/0092-8674(88)90111-0. [DOI] [PubMed] [Google Scholar]
  3. Amati B., Gasser S. M. Drosophila scaffold-attached regions bind nuclear scaffolds and can function as ARS elements in both budding and fission yeasts. Mol Cell Biol. 1990 Oct;10(10):5442–5454. doi: 10.1128/mcb.10.10.5442. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Avramova Z., Bennetzen J. L. Isolation of matrices from maize leaf nuclei: identification of a matrix-binding site adjacent to the Adh1 gene. Plant Mol Biol. 1993 Sep;22(6):1135–1143. doi: 10.1007/BF00028982. [DOI] [PubMed] [Google Scholar]
  5. Avramova Z., Paneva E. Matrix attachment sites in the murine alpha-globin gene. Biochem Biophys Res Commun. 1992 Jan 15;182(1):78–85. doi: 10.1016/s0006-291x(05)80114-7. [DOI] [PubMed] [Google Scholar]
  6. Avramova Z., SanMiguel P., Georgieva E., Bennetzen J. L. Matrix attachment regions and transcribed sequences within a long chromosomal continuum containing maize Adh1. Plant Cell. 1995 Oct;7(10):1667–1680. doi: 10.1105/tpc.7.10.1667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bode J., Kohwi Y., Dickinson L., Joh T., Klehr D., Mielke C., Kohwi-Shigematsu T. Biological significance of unwinding capability of nuclear matrix-associating DNAs. Science. 1992 Jan 10;255(5041):195–197. doi: 10.1126/science.1553545. [DOI] [PubMed] [Google Scholar]
  8. Bode J., Maass K. Chromatin domain surrounding the human interferon-beta gene as defined by scaffold-attached regions. Biochemistry. 1988 Jun 28;27(13):4706–4711. doi: 10.1021/bi00413a019. [DOI] [PubMed] [Google Scholar]
  9. Bode J., Pucher H. J., Maass K. Chromatin structure and induction-dependent conformational changes of human interferon-beta genes in a mouse host cell. Eur J Biochem. 1986 Jul 15;158(2):393–401. doi: 10.1111/j.1432-1033.1986.tb09766.x. [DOI] [PubMed] [Google Scholar]
  10. Bode J., Schlake T., Ríos-Ramírez M., Mielke C., Stengert M., Kay V., Klehr-Wirth D. Scaffold/matrix-attached regions: structural properties creating transcriptionally active loci. Int Rev Cytol. 1995;162A:389–454. doi: 10.1016/s0074-7696(08)61235-8. [DOI] [PubMed] [Google Scholar]
  11. Breyne P., Van Montagu M., Gheysen G. The role of scaffold attachment regions in the structural and functional organization of plant chromatin. Transgenic Res. 1994 May;3(3):195–202. doi: 10.1007/BF01973987. [DOI] [PubMed] [Google Scholar]
  12. Breyne P., van Montagu M., Depicker N., Gheysen G. Characterization of a plant scaffold attachment region in a DNA fragment that normalizes transgene expression in tobacco. Plant Cell. 1992 Apr;4(4):463–471. doi: 10.1105/tpc.4.4.463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Brun C., Dang Q., Miassod R. Studies of an 800-kilobase DNA stretch of the Drosophila X chromosome: comapping of a subclass of scaffold-attached regions with sequences able to replicate autonomously in Saccharomyces cerevisiae. Mol Cell Biol. 1990 Oct;10(10):5455–5463. doi: 10.1128/mcb.10.10.5455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Brun C., Surdej P., Miassod R. Relationship between scaffold-attached regions, sequences replicating autonomously in yeast, and a chromosomal replication origin in the Drosophila rDNA. Exp Cell Res. 1993 Sep;208(1):104–114. doi: 10.1006/excr.1993.1227. [DOI] [PubMed] [Google Scholar]
  15. Cai H., Levine M. Modulation of enhancer-promoter interactions by insulators in the Drosophila embryo. Nature. 1995 Aug 10;376(6540):533–536. doi: 10.1038/376533a0. [DOI] [PubMed] [Google Scholar]
  16. Carbone M. L., Solinas M., Sora S., Panzeri L. A gene tightly linked to CEN6 is important for growth of Saccharomyces cerevisiae. Curr Genet. 1991 Jan;19(1):1–8. doi: 10.1007/BF00362080. [DOI] [PubMed] [Google Scholar]
  17. Chung J. H., Whiteley M., Felsenfeld G. A 5' element of the chicken beta-globin domain serves as an insulator in human erythroid cells and protects against position effect in Drosophila. Cell. 1993 Aug 13;74(3):505–514. doi: 10.1016/0092-8674(93)80052-g. [DOI] [PubMed] [Google Scholar]
  18. Cockerill P. N., Garrard W. T. Chromosomal loop anchorage sites appear to be evolutionarily conserved. FEBS Lett. 1986 Aug 11;204(1):5–7. doi: 10.1016/0014-5793(86)81377-1. [DOI] [PubMed] [Google Scholar]
  19. Craddock C. F., Vyas P., Sharpe J. A., Ayyub H., Wood W. G., Higgs D. R. Contrasting effects of alpha and beta globin regulatory elements on chromatin structure may be related to their different chromosomal environments. EMBO J. 1995 Apr 18;14(8):1718–1726. doi: 10.1002/j.1460-2075.1995.tb07161.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Cunningham J. M., Purucker M. E., Jane S. M., Safer B., Vanin E. F., Ney P. A., Lowrey C. H., Nienhuis A. W. The regulatory element 3' to the A gamma-globin gene binds to the nuclear matrix and interacts with special A-T-rich binding protein 1 (SATB1), an SAR/MAR-associating region DNA binding protein. Blood. 1994 Aug 15;84(4):1298–1308. [PubMed] [Google Scholar]
  21. Dalrymple B. P., Peters J. M. Characterization of a cDNA clone from the haemoparasite Babesia bovis encoding a protein containing an "HMG-Box". Biochem Biophys Res Commun. 1992 Apr 15;184(1):31–35. doi: 10.1016/0006-291x(92)91153-h. [DOI] [PubMed] [Google Scholar]
  22. Dietz A., Kay V., Schlake T., Landsmann J., Bode J. A plant scaffold attached region detected close to a T-DNA integration site is active in mammalian cells. Nucleic Acids Res. 1994 Jul 25;22(14):2744–2751. doi: 10.1093/nar/22.14.2744. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Dorsett D. Distance-independent inactivation of an enhancer by the suppressor of Hairy-wing DNA-binding protein of Drosophila. Genetics. 1993 Aug;134(4):1135–1144. doi: 10.1093/genetics/134.4.1135. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Fackelmayer F. O., Dahm K., Renz A., Ramsperger U., Richter A. Nucleic-acid-binding properties of hnRNP-U/SAF-A, a nuclear-matrix protein which binds DNA and RNA in vivo and in vitro. Eur J Biochem. 1994 Apr 15;221(2):749–757. doi: 10.1111/j.1432-1033.1994.tb18788.x. [DOI] [PubMed] [Google Scholar]
  25. Fisscher U., Weisbeek P., Smeekens S. Identification of potential regulatory elements in the far-upstream region of the Arabidopsis thaliana plastocyanin promoter. Plant Mol Biol. 1994 Nov;26(3):873–886. doi: 10.1007/BF00028855. [DOI] [PubMed] [Google Scholar]
  26. Gasser S. M., Laemmli U. K. Cohabitation of scaffold binding regions with upstream/enhancer elements of three developmentally regulated genes of D. melanogaster. Cell. 1986 Aug 15;46(4):521–530. doi: 10.1016/0092-8674(86)90877-9. [DOI] [PubMed] [Google Scholar]
  27. Hall G., Jr, Allen G. C., Loer D. S., Thompson W. F., Spiker S. Nuclear scaffolds and scaffold-attachment regions in higher plants. Proc Natl Acad Sci U S A. 1991 Oct 15;88(20):9320–9324. doi: 10.1073/pnas.88.20.9320. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Hardwick K. G., Pelham H. R. SED6 is identical to ERG6, and encodes a putative methyltransferase required for ergosterol synthesis. Yeast. 1994 Feb;10(2):265–269. doi: 10.1002/yea.320100213. [DOI] [PubMed] [Google Scholar]
  29. Herrscher R. F., Kaplan M. H., Lelsz D. L., Das C., Scheuermann R., Tucker P. W. The immunoglobulin heavy-chain matrix-associating regions are bound by Bright: a B cell-specific trans-activator that describes a new DNA-binding protein family. Genes Dev. 1995 Dec 15;9(24):3067–3082. doi: 10.1101/gad.9.24.3067. [DOI] [PubMed] [Google Scholar]
  30. Holmgren A. Thioredoxin and glutaredoxin systems. J Biol Chem. 1989 Aug 25;264(24):13963–13966. [PubMed] [Google Scholar]
  31. Izaurralde E., Mirkovitch J., Laemmli U. K. Interaction of DNA with nuclear scaffolds in vitro. J Mol Biol. 1988 Mar 5;200(1):111–125. doi: 10.1016/0022-2836(88)90337-3. [DOI] [PubMed] [Google Scholar]
  32. Jackson D. A., Dickinson P., Cook P. R. The size of chromatin loops in HeLa cells. EMBO J. 1990 Feb;9(2):567–571. doi: 10.1002/j.1460-2075.1990.tb08144.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Jones S. W., Luk K. C. Isolation of a chicken thioredoxin cDNA clone. Thioredoxin mRNA is differentially expressed in normal and Rous sarcoma virus-transformed chicken embryo fibroblasts. J Biol Chem. 1988 Jul 15;263(20):9607–9611. [PubMed] [Google Scholar]
  34. Kellum R., Schedl P. A group of scs elements function as domain boundaries in an enhancer-blocking assay. Mol Cell Biol. 1992 May;12(5):2424–2431. doi: 10.1128/mcb.12.5.2424. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Klehr D., Maass K., Bode J. Scaffold-attached regions from the human interferon beta domain can be used to enhance the stable expression of genes under the control of various promoters. Biochemistry. 1991 Feb 5;30(5):1264–1270. doi: 10.1021/bi00219a015. [DOI] [PubMed] [Google Scholar]
  36. Kolodrubetz D., Burgum A. Duplicated NHP6 genes of Saccharomyces cerevisiae encode proteins homologous to bovine high mobility group protein 1. J Biol Chem. 1990 Feb 25;265(6):3234–3239. [PubMed] [Google Scholar]
  37. Kun J. F., Anders R. F. A Plasmodium falciparum gene encoding a high mobility group protein box. Mol Biochem Parasitol. 1995 May;71(2):249–253. doi: 10.1016/0166-6851(94)00047-q. [DOI] [PubMed] [Google Scholar]
  38. Laemmli U. K., Käs E., Poljak L., Adachi Y. Scaffold-associated regions: cis-acting determinants of chromatin structural loops and functional domains. Curr Opin Genet Dev. 1992 Apr;2(2):275–285. doi: 10.1016/s0959-437x(05)80285-0. [DOI] [PubMed] [Google Scholar]
  39. Levy-Wilson B., Fortier C. The limits of the DNase I-sensitive domain of the human apolipoprotein B gene coincide with the locations of chromosomal anchorage loops and define the 5' and 3' boundaries of the gene. J Biol Chem. 1989 Dec 15;264(35):21196–21204. [PubMed] [Google Scholar]
  40. Ludérus M. E., de Graaf A., Mattia E., den Blaauwen J. L., Grande M. A., de Jong L., van Driel R. Binding of matrix attachment regions to lamin B1. Cell. 1992 Sep 18;70(6):949–959. doi: 10.1016/0092-8674(92)90245-8. [DOI] [PubMed] [Google Scholar]
  41. Mirkovitch J., Gasser S. M., Laemmli U. K. Scaffold attachment of DNA loops in metaphase chromosomes. J Mol Biol. 1988 Mar 5;200(1):101–109. doi: 10.1016/0022-2836(88)90336-1. [DOI] [PubMed] [Google Scholar]
  42. Mirkovitch J., Mirault M. E., Laemmli U. K. Organization of the higher-order chromatin loop: specific DNA attachment sites on nuclear scaffold. Cell. 1984 Nov;39(1):223–232. doi: 10.1016/0092-8674(84)90208-3. [DOI] [PubMed] [Google Scholar]
  43. Mirkovitch J., Spierer P., Laemmli U. K. Genes and loops in 320,000 base-pairs of the Drosophila melanogaster chromosome. J Mol Biol. 1986 Jul 20;190(2):255–258. doi: 10.1016/0022-2836(86)90296-2. [DOI] [PubMed] [Google Scholar]
  44. Mlynarova L., Jansen R. C., Conner A. J., Stiekema W. J., Nap J. P. The MAR-Mediated Reduction in Position Effect Can Be Uncoupled from Copy Number-Dependent Expression in Transgenic Plants. Plant Cell. 1995 May;7(5):599–609. doi: 10.1105/tpc.7.5.599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Nakagomi K., Kohwi Y., Dickinson L. A., Kohwi-Shigematsu T. A novel DNA-binding motif in the nuclear matrix attachment DNA-binding protein SATB1. Mol Cell Biol. 1994 Mar;14(3):1852–1860. doi: 10.1128/mcb.14.3.1852. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Paranjape S. M., Kamakaka R. T., Kadonaga J. T. Role of chromatin structure in the regulation of transcription by RNA polymerase II. Annu Rev Biochem. 1994;63:265–297. doi: 10.1146/annurev.bi.63.070194.001405. [DOI] [PubMed] [Google Scholar]
  47. Paull T. T., Johnson R. C. DNA looping by Saccharomyces cerevisiae high mobility group proteins NHP6A/B. Consequences for nucleoprotein complex assembly and chromatin condensation. J Biol Chem. 1995 Apr 14;270(15):8744–8754. doi: 10.1074/jbc.270.15.8744. [DOI] [PubMed] [Google Scholar]
  48. Pruitt R. E., Meyerowitz E. M. Characterization of the genome of Arabidopsis thaliana. J Mol Biol. 1986 Jan 20;187(2):169–183. doi: 10.1016/0022-2836(86)90226-3. [DOI] [PubMed] [Google Scholar]
  49. Quaedvlieg N., Dockx J., Rook F., Weisbeek P., Smeekens S. The homeobox gene ATH1 of Arabidopsis is derepressed in the photomorphogenic mutants cop1 and det1. Plant Cell. 1995 Jan;7(1):117–129. doi: 10.1105/tpc.7.1.117. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Razin S. V., Hancock R., Iarovaia O., Westergaard O., Gromova I., Georgiev G. P. Structural-functional organization of chromosomal DNA domains. Cold Spring Harb Symp Quant Biol. 1993;58:25–35. doi: 10.1101/sqb.1993.058.01.006. [DOI] [PubMed] [Google Scholar]
  51. Razin S. V., Petrov P., Hancock R. Precise localization of the alpha-globin gene cluster within one of the 20- to 300-kilobase DNA fragments released by cleavage of chicken chromosomal DNA at topoisomerase II sites in vivo: evidence that the fragments are DNA loops or domains. Proc Natl Acad Sci U S A. 1991 Oct 1;88(19):8515–8519. doi: 10.1073/pnas.88.19.8515. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Roberge M., Gasser S. M. DNA loops: structural and functional properties of scaffold-attached regions. Mol Microbiol. 1992 Feb;6(4):419–423. doi: 10.1111/j.1365-2958.1992.tb01485.x. [DOI] [PubMed] [Google Scholar]
  53. Slatter R. E., Dupree P., Gray J. C. A scaffold-associated DNA region is located downstream of the pea plastocyanin gene. Plant Cell. 1991 Nov;3(11):1239–1250. doi: 10.1105/tpc.3.11.1239. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Spana C., Harrison D. A., Corces V. G. The Drosophila melanogaster suppressor of Hairy-wing protein binds to specific sequences of the gypsy retrotransposon. Genes Dev. 1988 Nov;2(11):1414–1423. doi: 10.1101/gad.2.11.1414. [DOI] [PubMed] [Google Scholar]
  55. Surdej P., Brandli D., Miassod R. Scaffold-associated regions and repeated or cross-hybridizing sequences on an 800 kilobase DNA stretch of the Drosophila X chromosome. Biol Cell. 1991;73(2-3):111–120. doi: 10.1016/0248-4900(91)90093-3. [DOI] [PubMed] [Google Scholar]
  56. Surdej P., Got C., Rosset R., Miassod R. Supragenic loop organization: mapping in Drosophila embryos, of scaffold-associated regions on a 800 kilobase DNA continuum cloned from the 14B-15B first chromosome region. Nucleic Acids Res. 1990 Jul 11;18(13):3713–3722. doi: 10.1093/nar/18.13.3713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Talbot D., Descombes P., Schibler U. The 5' flanking region of the rat LAP (C/EBP beta) gene can direct high-level, position-independent, copy number-dependent expression in multiple tissues in transgenic mice. Nucleic Acids Res. 1994 Mar 11;22(5):756–766. doi: 10.1093/nar/22.5.756. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Tonissen K. F., Wells J. R. Isolation and characterization of human thioredoxin-encoding genes. Gene. 1991 Jun 30;102(2):221–228. doi: 10.1016/0378-1119(91)90081-l. [DOI] [PubMed] [Google Scholar]
  59. Udvardy A., Maine E., Schedl P. The 87A7 chromomere. Identification of novel chromatin structures flanking the heat shock locus that may define the boundaries of higher order domains. J Mol Biol. 1985 Sep 20;185(2):341–358. doi: 10.1016/0022-2836(85)90408-5. [DOI] [PubMed] [Google Scholar]
  60. Vorst O., Kock P., Lever A., Weterings B., Weisbeek P., Smeekens S. The promoter of the Arabidopsis thaliana plastocyanin gene contains a far upstream enhancer-like element involved in chloroplast-dependent expression. Plant J. 1993 Dec;4(6):933–945. doi: 10.1046/j.1365-313x.1993.04060933.x. [DOI] [PubMed] [Google Scholar]
  61. Vorst O., Oosterhoff-Teertstra R., Vankan P., Smeekens S., Weisbeek P. Plastocyanin of Arabidopsis thaliana; isolation and characterization of the gene and chloroplast import of the precursor protein. Gene. 1988 May 15;65(1):59–69. doi: 10.1016/0378-1119(88)90417-9. [DOI] [PubMed] [Google Scholar]
  62. Wilson R., Ainscough R., Anderson K., Baynes C., Berks M., Bonfield J., Burton J., Connell M., Copsey T., Cooper J. 2.2 Mb of contiguous nucleotide sequence from chromosome III of C. elegans. Nature. 1994 Mar 3;368(6466):32–38. doi: 10.1038/368032a0. [DOI] [PubMed] [Google Scholar]
  63. Wolffe A. P. New insights into chromatin function in transcriptional control. FASEB J. 1992 Dec;6(15):3354–3361. doi: 10.1096/fasebj.6.15.1464369. [DOI] [PubMed] [Google Scholar]
  64. Wollman E. E., d'Auriol L., Rimsky L., Shaw A., Jacquot J. P., Wingfield P., Graber P., Dessarps F., Robin P., Galibert F. Cloning and expression of a cDNA for human thioredoxin. J Biol Chem. 1988 Oct 25;263(30):15506–15512. [PubMed] [Google Scholar]
  65. Zhao K., Hart C. M., Laemmli U. K. Visualization of chromosomal domains with boundary element-associated factor BEAF-32. Cell. 1995 Jun 16;81(6):879–889. doi: 10.1016/0092-8674(95)90008-x. [DOI] [PubMed] [Google Scholar]

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