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. 1995 Nov;7(11):1923–1932. doi: 10.1105/tpc.7.11.1923

The Arabidopsis Adh gene exhibits diverse nucleosome arrangements within a small DNase I-sensitive domain.

M A Vega-Palas 1, R J Ferl 1
PMCID: PMC161050  PMID: 8535143

Abstract

The alcohol dehydrogenase (Adh) gene from Arabidopsis shows enhanced sensitivity to DNase I in cells that express the gene. This generalized sensitivity to DNase I is demarcated by position -500 on the 5' side and the end of the mRNA on the 3' side. Thus, the gene defined as the promoter and mRNA coding region corresponds very closely in size with the gene defined as a nuclease-sensitive domain. This is a remarkably close correspondence between a sensitive domain and a eukaryotic transcriptional unit, because previously reported DNase I-sensitive domains include large regions of DNA that are not transcribed. Nucleosomes are present in the coding region of the Adh gene when it is expressed, indicating that the transcriptional elongation process causes nucleosome disruption rather than release of nucleosomes from the coding region. In addition, the regulatory region contains a loosely positioned nucleosome that is separated from adjacent nucleosomes by internucleosomic DNA segments longer than the average linker DNA in bulk chromatin. This specific array of nucleosomes coexists with bound transcription factors that could contribute to the organization of the nucleosome arrangement. These results enhance our understanding of the complex interactions among DNA, nucleosomes, and transcription factors during gene expression in plants.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adams C. C., Workman J. L. Nucleosome displacement in transcription. Cell. 1993 Feb 12;72(3):305–308. doi: 10.1016/0092-8674(93)90109-4. [DOI] [PubMed] [Google Scholar]
  2. Almer A., Hörz W. Nuclease hypersensitive regions with adjacent positioned nucleosomes mark the gene boundaries of the PHO5/PHO3 locus in yeast. EMBO J. 1986 Oct;5(10):2681–2687. doi: 10.1002/j.1460-2075.1986.tb04551.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Almer A., Rudolph H., Hinnen A., Hörz W. Removal of positioned nucleosomes from the yeast PHO5 promoter upon PHO5 induction releases additional upstream activating DNA elements. EMBO J. 1986 Oct;5(10):2689–2696. doi: 10.1002/j.1460-2075.1986.tb04552.x. [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. Bellard M., Kuo M. T., Dretzen G., Chambon P. Differential nuclease sensitivity of the ovalbumin and beta-globin chromatin regions in erythrocytes and oviduct cells of laying hen. Nucleic Acids Res. 1980 Jun 25;8(12):2737–2750. doi: 10.1093/nar/8.12.2737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Buratowski S. The basics of basal transcription by RNA polymerase II. Cell. 1994 Apr 8;77(1):1–3. doi: 10.1016/0092-8674(94)90226-7. [DOI] [PubMed] [Google Scholar]
  7. Chang C., Meyerowitz E. M. Molecular cloning and DNA sequence of the Arabidopsis thaliana alcohol dehydrogenase gene. Proc Natl Acad Sci U S A. 1986 Mar;83(5):1408–1412. doi: 10.1073/pnas.83.5.1408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chodosh L. A., Buratowski S., Sharp P. A. A yeast protein possesses the DNA-binding properties of the adenovirus major late transcription factor. Mol Cell Biol. 1989 Feb;9(2):820–822. doi: 10.1128/mcb.9.2.820. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Clark D. J., Kimura T. Electrostatic mechanism of chromatin folding. J Mol Biol. 1990 Feb 20;211(4):883–896. doi: 10.1016/0022-2836(90)90081-V. [DOI] [PubMed] [Google Scholar]
  10. Conconi A., Ryan C. A. DNase I and micrococcal nuclease analysis of the tomato proteinase inhibitor I gene in chromatin. J Biol Chem. 1993 Jan 5;268(1):430–435. [PubMed] [Google Scholar]
  11. Conconi A., Widmer R. M., Koller T., Sogo J. M. Two different chromatin structures coexist in ribosomal RNA genes throughout the cell cycle. Cell. 1989 Jun 2;57(5):753–761. doi: 10.1016/0092-8674(89)90790-3. [DOI] [PubMed] [Google Scholar]
  12. Dolferus R., Jacobs M., Peacock W. J., Dennis E. S. Differential interactions of promoter elements in stress responses of the Arabidopsis Adh gene. Plant Physiol. 1994 Aug;105(4):1075–1087. doi: 10.1104/pp.105.4.1075. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Donald R. G., Schindler U., Batschauer A., Cashmore A. R. The plant G box promoter sequence activates transcription in Saccharomyces cerevisiae and is bound in vitro by a yeast activity similar to GBF, the plant G box binding factor. EMBO J. 1990 Jun;9(6):1727–1735. doi: 10.1002/j.1460-2075.1990.tb08296.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Elgin S. C. The formation and function of DNase I hypersensitive sites in the process of gene activation. J Biol Chem. 1988 Dec 25;263(36):19259–19262. [PubMed] [Google Scholar]
  15. Felsenfeld G. Chromatin as an essential part of the transcriptional mechanism. Nature. 1992 Jan 16;355(6357):219–224. doi: 10.1038/355219a0. [DOI] [PubMed] [Google Scholar]
  16. Ferl R. J., Nick H. S. In vivo detection of regulatory factor binding sites in the 5' flanking region of maize Adh1. J Biol Chem. 1987 Jun 15;262(17):7947–7950. [PubMed] [Google Scholar]
  17. Frommer W. B., Starlinger P. DNase I hypersensitive sites in the 5'-region of the maize Shrunken gene in nuclei from different organs. Mol Gen Genet. 1988 May;212(2):351–359. doi: 10.1007/BF00334706. [DOI] [PubMed] [Google Scholar]
  18. Jantzen K., Fritton H. P., Igo-Kemenes T. The DNase I sensitive domain of the chicken lysozyme gene spans 24 kb. Nucleic Acids Res. 1986 Aug 11;14(15):6085–6099. doi: 10.1093/nar/14.15.6085. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kaufman L. S., Watson J. C., Thompson W. F. Light-regulated changes in DNase I hypersensitive sites in the rRNA genes of Pisum sativum. Proc Natl Acad Sci U S A. 1987 Mar;84(6):1550–1554. doi: 10.1073/pnas.84.6.1550. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Keene M. A., Elgin S. C. Micrococcal nuclease as a probe of DNA sequence organization and chromatin structure. Cell. 1981 Nov;27(1 Pt 2):57–64. doi: 10.1016/0092-8674(81)90360-3. [DOI] [PubMed] [Google Scholar]
  21. Kornberg R. D., Lorch Y. Irresistible force meets immovable object: transcription and the nucleosome. Cell. 1991 Nov 29;67(5):833–836. doi: 10.1016/0092-8674(91)90354-2. [DOI] [PubMed] [Google Scholar]
  22. Lawson G. M., Knoll B. J., March C. J., Woo S. L., Tsai M. J., O'Malley B. W. Definition of 5' and 3' structural boundaries of the chromatin domain containing the ovalbumin multigene family. J Biol Chem. 1982 Feb 10;257(3):1501–1507. [PubMed] [Google Scholar]
  23. 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]
  24. Loc P. V., Strätling W. H. The matrix attachment regions of the chicken lysozyme gene co-map with the boundaries of the chromatin domain. EMBO J. 1988 Mar;7(3):655–664. doi: 10.1002/j.1460-2075.1988.tb02860.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. McKendree W. L., Jr, Ferl R. J. Functional elements of the Arabidopsis Adh promoter include the G-box. Plant Mol Biol. 1992 Aug;19(5):859–862. doi: 10.1007/BF00027081. [DOI] [PubMed] [Google Scholar]
  26. McKendree W. L., Paul A. L., DeLisle A. J., Ferl R. J. In vivo and in vitro characterization of protein interactions with the dyad G-box of the Arabidopsis Adh gene. Plant Cell. 1990 Mar;2(3):207–214. doi: 10.1105/tpc.2.3.207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. 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]
  29. Paul A. L., Ferl R. J. Osmium tetroxide footprinting of a scaffold attachment region in the maize Adh1 promoter. Plant Mol Biol. 1993 Sep;22(6):1145–1151. doi: 10.1007/BF00028983. [DOI] [PubMed] [Google Scholar]
  30. Paul A. L., Vasil V., Vasil I. K., Ferl R. J. Constitutive and anaerobically induced DNase-I-hypersensitive sites in the 5' region of the maize Adh1 gene. Proc Natl Acad Sci U S A. 1987 Feb;84(3):799–803. doi: 10.1073/pnas.84.3.799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Piña B., Brüggemeier U., Beato M. Nucleosome positioning modulates accessibility of regulatory proteins to the mouse mammary tumor virus promoter. Cell. 1990 Mar 9;60(5):719–731. doi: 10.1016/0092-8674(90)90087-u. [DOI] [PubMed] [Google Scholar]
  32. Schindler U., Terzaghi W., Beckmann H., Kadesch T., Cashmore A. R. DNA binding site preferences and transcriptional activation properties of the Arabidopsis transcription factor GBF1. EMBO J. 1992 Apr;11(4):1275–1289. doi: 10.1002/j.1460-2075.1992.tb05171.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Stalder J., Larsen A., Engel J. D., Dolan M., Groudine M., Weintraub H. Tissue-specific DNA cleavages in the globin chromatin domain introduced by DNAase I. Cell. 1980 Jun;20(2):451–460. doi: 10.1016/0092-8674(80)90631-5. [DOI] [PubMed] [Google Scholar]
  34. Storb U., Wilson R., Selsing E., Walfield A. Rearranged and germline immunoglobulin kappa genes: different states of DNase I sensitivity of constant kappa genes in immunocompetent and nonimmune cells. Biochemistry. 1981 Feb 17;20(4):990–996. doi: 10.1021/bi00507a053. [DOI] [PubMed] [Google Scholar]
  35. Thompson W. F., Flavell R. B. DNase I sensitivity of ribosomal RNA genes in chromatin and nucleolar dominance in wheat. J Mol Biol. 1988 Dec 5;204(3):535–548. doi: 10.1016/0022-2836(88)90353-1. [DOI] [PubMed] [Google Scholar]
  36. Tjian R., Maniatis T. Transcriptional activation: a complex puzzle with few easy pieces. Cell. 1994 Apr 8;77(1):5–8. doi: 10.1016/0092-8674(94)90227-5. [DOI] [PubMed] [Google Scholar]
  37. Tsukiyama T., Becker P. B., Wu C. ATP-dependent nucleosome disruption at a heat-shock promoter mediated by binding of GAGA transcription factor. Nature. 1994 Feb 10;367(6463):525–532. doi: 10.1038/367525a0. [DOI] [PubMed] [Google Scholar]
  38. Walker J. C., Howard E. A., Dennis E. S., Peacock W. J. DNA sequences required for anaerobic expression of the maize alcohol dehydrogenase 1 gene. Proc Natl Acad Sci U S A. 1987 Oct;84(19):6624–6628. doi: 10.1073/pnas.84.19.6624. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Weintraub H., Groudine M. Chromosomal subunits in active genes have an altered conformation. Science. 1976 Sep 3;193(4256):848–856. doi: 10.1126/science.948749. [DOI] [PubMed] [Google Scholar]
  40. Williams M. E., Foster R., Chua N. H. Sequences flanking the hexameric G-box core CACGTG affect the specificity of protein binding. Plant Cell. 1992 Apr;4(4):485–496. doi: 10.1105/tpc.4.4.485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Wolffe A. P. Transcription: in tune with the histones. Cell. 1994 Apr 8;77(1):13–16. doi: 10.1016/0092-8674(94)90229-1. [DOI] [PubMed] [Google Scholar]
  42. Wood W. I., Felsenfeld G. Chromatin structure of the chicken beta-globin gene region. Sensitivity to DNase I, micrococcal nuclease, and DNase II. J Biol Chem. 1982 Jul 10;257(13):7730–7736. [PubMed] [Google Scholar]
  43. Wu C. The 5' ends of Drosophila heat shock genes in chromatin are hypersensitive to DNase I. Nature. 1980 Aug 28;286(5776):854–860. doi: 10.1038/286854a0. [DOI] [PubMed] [Google Scholar]
  44. van Holde K. E., Lohr D. E., Robert C. What happens to nucleosomes during transcription? J Biol Chem. 1992 Feb 15;267(5):2837–2840. [PubMed] [Google Scholar]

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