A short synthetic MAR positively affects transgene expression in rice and Arabidopsis

Plant Biotechnology Journal

Volumn 2, Issue 1, 2004, Pages 13-26

  Van Der Geest, Apolonia H M ^a   Welter, Mary E ^a   Woosley, Aaron T ^a   Pareddy, Dayakar R ^a   Pavelko, Sarah E ^a   Skokut, Michiyo ^a   Ainley, William M ^a  

^a Dow Agro Sciences   (United States)

Author keywords

MARs; Matrix attachment regions; Transgene locus complexity

Indexed keywords

ARABIDOPSIS; EMBRYOPHYTA; EUKARYOTA;

EID: 13444291411     PISSN: 14677644     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1467-7652.2003.00044.x     Document Type: Article

References (74)

1. Allen, G.C., Hall Jr, G.E., Childs, L.C., Weissinger, A.K., Spiker, S. and Thompson, W.F. (1993) Scaffold attachment regions increase reporter gene expression in stably transformed plant cells. Plant Cell, 5, 603-613.
2. Allen, G.C., Hall Jr, G.E., Michalowski, S., Newman, W., Spiker, S., Weissinger, A.K. and Thompson, W.F. (1996) High-level transgene expression in plant cells: effects of a strong scaffold attachment region from tobacco. Plant Cell, 8, 899-913.
3. Allen, G.C., Spiker, S. and Thompson, W.F. (2000) Use of matrix attachment regions (MARs) to minimize transgene silencing. Plant Mol. Biol. 43, 361-376.
4. An, Y.-Q., McDowell, J.M., Huang, S., McKinney, E.C., Chambliss, S. and Meagher, R.B. (1996) Strong constitutive expression of the Arabidopsis ACT2/ACT8 actin subclass in vegetative tissues. Plant J. 10, 107-121.
5. Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A. and Struhl, K., eds. (2000) Current Protocols in Molecular Biology. New Jersey: John Wiley & Sons.
6. Avramova, Z. and Bennetzen, J.L. (1993) Isolation of matrices from maize leaf nuclei: identification of a matrix-binding site adjacent to the Adh1 gene. Plant Mol. Biol. 22, 1135-1143.
7. Avramova, Z., SanMiguel, P., Georgieva, E. and Bennetzen, J.L. (1995) Matrix attachment regions and transcribed sequences within a long chromosomal continuum containing maize Adh1. Plant Cell, 7, 1667-1680.
8. Benham, C., Kohwi-Shigematsu, T. and Bode, J. (1997) Stress-induced duplex DNA destabilization in scaffold/matrix attachment regions. J. Mol. Biol. 274, 181-196.
9. Bode, J., Kohwi, Y., Dickinson, L., Joh, Y., Klehr, D., Mielke, C. and Kohwi-Shigematsu, T. (1992) Biological significance of unwinding capability of nuclear matrix-associated DNAs. Science, 255, 195-197.
10. Bode, J., Schlake, T., Rios-Ramirez, M., Mielke, C., Stengert, M., Kay, V. and Klehr-Wirth, D. (1995) Scaffold/matrix-attached regions: Structural properties creating transcriptionally active loci. Int. Rev. Cytol. 162A, 389-454.
11. Boulikas, T. (1995) Chromatin domains and the prediction of MAR sequences. Int. Rev. Cytol. 162A, 279-388.
12. Boulikas, T. and Kong, C.F. (1993) Multitude of inverted repeats characterize a class of anchorage sites of chromatin loops to the nuclear matrix. J. Cell. Biochem. 53, 1-12.
13. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
14. Breyne, P., Van Montagu, M., Depicker, A. and Gheysen, G. (1992) Characterization of a plant scaffold attachment region in a DNA fragment that normalizes transgene expression in tobacco. Plant Cell, 4, 463-471.
15. Breyne, P., van Montagu, M. and Gheysen, G. (1994) The role of scaffold attachment regions in the structural and functional organization of plant chromatin. Transgenic Res. 3, 195-202.
16. Brouwer, C., Bruce, W., Maddock, S., Avramova, Z. and Bowen, B. (2003) Suppression of transgene silencing by matrix attachment regions in maize, a dual role for the maize 5́-ADH1 matrix attachment region. Plant Cell, 14, 2251-2264.
17. Buhrmester, H., von Kries, J.P. and Stratling, W.H. (1995) Nuclear matrix protein ARBP recognizes a novel DNA sequence motif with high affinity. Biochemistry, 34, 4108-4117.
18. Chen, L., Zhang, S., Beachy, R.N. and Fauquet, C.M. (1998) A protocol for consistent, large-scale production of fertile transgenic rice plants. Plant Cell Rep. 18, 25-31.
19. Depicker, A., Stachel, S., Dhaese, P., Zambryski, P. and Goodman, H.M. (1982) Nopaline Synthase: Transcript mapping and DNA sequence. J. Molec. Appl. Genet. 1, 561-573.
20. Dickinson, L.A., Joh, T., Kohwi, Y. and Kohwi-Shigematsu, T. (1992) A tissue-specific MAR/SAR DNA-binding protein with unusual binding site recognition. Cell, 70, 631-645.
21. Dietz, A., Volker, K., Schlake, T., Landsmann, J. and Bode, J. (1994) A plant scaffold attached region detected close to a T-DNA integration site is active in mammalian cells. Nucl. Acids Res. 22, 2744-2751.
22. Dillon, N. and Grosveld, F. (1994) Chromatin domains as potential units of eukaryotic gene function. Curr. Opin. Gen. Dev. 4, 260-264.
23. van Drunen, C.M., Oosterling, R.W., Keultjes, G.M., Weisbeek, P.J., Smeekens, S.C.M. and van Driel, R. (1999) A bipartite sequence element associated with matrix/scaffold attachment regions. Nucl. Acids Res. 27, 2924-2930.
24. van Drunen, C.M., Sewalt, R.G.A.B., Oosterling, R.W., Weisbeek, P.J., van Driel, R. and Smeekens, S.C.M. (1997) Analysis of the chromatin domain organisation around the plastocyanin gene reveals an MAR-specific sequence element in Arabidopsis thaliana. Nucl. Acids Res. 25, 3904-3911.
25. Finnegan, J. and McElroy, D. (1994) Transgene inactivation: plants fight back! Biotechnology, 12, 883-888.
26. Fukuda, Y. (2000) Interaction of nuclear proteins with intrinsically curved DNA in a matrix attachment region of a tobacco gene. Plant Mol. Biol. 44, 91-98.
27. Gallie, D.R. (1998) Controlling gene expression in transgenic plants. Curr. Opin. Plant Biol. 1, 166-172.
28. Gamborg, O.L., Miller, R.A. and Ojima, K. (1968) Nutrient requirements of suspension cultures of soybean root cells. J. Exp. Res. 50, 151-158.
29. van der Geest, A.M.M., Hall Jr G.E., Spiker, S. and Hall, T.C. (1994) The beta-phaseolin gene is flanked by matrix attachment regions. Plant J. 6, 413-423.
30. Glazko, G.V., Rogozin, I.B. and Glazkov, M.V. (2000) Computer prediction of DNA sites of attachment to different nuclear matrix elements. Mol. Biol. 34, 1-5.
31. Glazko, G.V., Rogozin, I.B. and Glazkov, M.V. (2001) Comparative study and prediction of DNA fragments associated with various element of the nuclear matrix. Biochem. Biophys. Acta, 1517, 351-364.
32. Hagerman, P.J. (1990) Sequence-directed curvature of DNA. Annu. Rev. Biochem. 59, 755-781.
33. Hall, G. Jr, Allen, G.C., Loer, D.S., Thompson, W.F. and Spiker, S. (1991) Nuclear scaffolds and scaffold-attachment regions in higher plants. Proc. Natl Acad. Sci. USA, 88, 9320-9324.
34. Holmes-Davis, R. and Comai, L. (1998) Nuclear matrix attachment regions and plant gene expression. Trends Plant Sci. 3, 91-97.
35. van Hoof, A. and Green, P. (1996) Premature nonsense codons decrease the stability of phytohemagglutinin mRNA in a position-dependent manner. Plant J. 10, 415-424.
36. Iyer, L.M., Kumpatla, S.P., Chandrasekharan, M.B. and Hall, T.C. (2000) Transgene silencing in monocots. Plant. Mol. Biol. 43, 323-346.
37. Jackson, D.A. (1995) Nuclear organization: uniting replication foci, chromatin domains and chromosome structure. Bioessays, 17, 587-591.
38. Jefferson, R.A. (1987) Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol. Biol. Rep. 5, 387-405.
39. Jefferson, R.A., Burgess, S.M. and Hirsh, D. (1986) β-Glucuronidase from Escherichia coli as a gene-fusion marker. Proc Natl Acad. Sci. USA 83, 847-8451.
40. Kohli, A., Griffiths, S., Palacios, N., Twyman, R.M., Vain, P., Laurie, D.A. and Christou, P. (1999) Molecular characterization of tranforming plasmid rearrangements in transgene rice reveals a recombination hotspot in the CaMV 35S promoter and confirms the predominance of microhomology mediated recombination. Plant J. 1, 591-601.
41. Kohli, A., Leech, M., Vain, P., Laurie, D.A. and Christou, P. (1998) Transgene organization in rice engineered through direct DNA transfer supports a two-phase integration mechanism mediated by the establishment of integration hot spots. Proc. Natl Acad. Sci. USA, 9, 7203-7208.
42. von Kries, J.P., Buhrmester, H. and Strätling, W.H. (1991) A matrix/ scaffold attachment region binding protein: Identification, purification and mode of binding. Cell, 64, 123-135.
43. Kriz, A.L., Boston, R.S. and Larkins, B.A. (1987) Structural and transcriptional analysis of DNA sequences flanking genes that encode 19 kilodalton zeins. Mol. Gen. Genet. 207, 90-98.
44. Kumpatla, S.P., Chandrasekharan, M.B., Iyer, L.M., Li, G. and Hall, T.C. (1998) Genome intruder scanning and modulation systems and transgene silencing. Trends Plant Sci. 3, 97-104.
45. Lewin, B. (1994) Chromatin and gene expression: Constant questions, but changing answers. Cell, 79, 397-406.
46. Li, L., Qu, R., de Kochko, A., Fauquet, C. and Beachy, R.N. (1993) An improved rice transformation system using the biolistic method. Plant Cell Rep. 12, 250-255.
47. Liu, J.-W. and Tabe, L.M. (1998) The influences of two plant nuclear matrix attachment regions (MARs) on gene expression in transgenic plants. Plant Cell Physiol. 39, 115-123.
48. Matzke, A.J.M. and Matzke, M.A. (1998) Position effects and epigenetic silencing of plant transgenes. Curr. Opin. Plant Biol. 1, 142-148.
49. Michalowski, S.M., Allen, G.C. Hall Jr, G.E., Thompson, W.F. and Spiker, S. (1999) Characterization of randomly-obtained matrix attachment regions (MARs) from higher plants. Biochemistry, 38, 12795-12804.
50. Mlynárová, L., Jansen, R.C., Conner, A.J., Stiekema, W.J. and Nap, J.-P. (1995) The MAR-mediated reduction in position effect can be uncoupled from copy number-dependent expression in transgenic plants. Plant Cell, 7, 599-609.
51. Mlynárová, L., Loonen, A., Heldens, J., Jansen, R.C., Keizer, P., Stiekema, W.J. and Nap, J.-P. (1994) Reduced position effect in mature transgenic plants conferred by the chicken lysozyme matrix-associated region. Plant Cell, 6, 417-426.
52. Muskens, M.W.M., Vissers, A.P.A., Mol, J.N.M. and Kooter, J.M. (2000) Role of inverted DNA repeats in transcriptional and posttranscriptional gene silencing. Plant Mol. Biol. 43, 243-260.
53. Nagagomi, K., Kohwi, Y., Dickinson, L.A. and Kohwi-Shigematsu, T. (1994) A novel DNA binding motif in the nuclear matrix attachment binding protein SATB1. Mol. Cell. Biol. 14, 1852-1860.
54. Nowak, W., Gawlowska, M., Jarmolowski, A. and Augustyniak, J. (2001) Effect of nuclear matrix attachment regions on transgene expression in tobacco plants. Acta Bioch. Polonica, 48, 637-646.
55. Pareddy, D., Petolino, J., Skokut, T., Hopkins, N., Miller, M., Welter, M., Smith, K., Clayton, D., Pescitelli, S. and Gould, A. (1997) Maize transformation via helium blasting. Maydica, 42, 143-154.
56. de Pater, B.S., van der Mark, F., Rueb, S., Katagiri, F., Chua, N.-H., Schilperoort, R.A. and Hensgens, L.A.M. (1992) The promoter of the rice gene GOS2 is active in various different monocot tissues and binds rice nuclear factor ASF-1. Plant J. 2, 837-844.
57. Quigley, F., Brinkmann, H., Martin, W.F. and Cerff, R. (1989) Strong functional GC pressure in a light-regulated maize gene encoding subunit GAPA of chloroplast glyceraldehyde-3-phosphate dehydrogenase. implications for the evolution of GAPA pseudogenes. J. Mol. Biol. 29, 412-421.
58. Romig, H., Fackelmayer, F.O., Renz, A., Ramsperger, U. and Richter, A. (1992) Characterization of SAF-A, a novel nuclear DNA binding protein from HeLa cells with high affinity for nuclear matrix/scaffold attachment DNA elements. EMBO J. 11, 3431-3440.
59. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
60. Sander, M. and Hsieh, T.-S. (1985) Drosophila topoisomerase II double-strand cleavage: Analysis of DNA sequence homology at the cleavage site. Nucl. Acids Res. 13, 1057-1072.
61. Schöffl, F., Schröder, G., Kliem, M. and Rieping, M. (1993) An SAR sequence containing 395 bp DNA fragment mediates enhanced, gene-dosage-correlated expression of a chimaeric heat shock gene in transgenic tobacco plants. Transgenic Res. 2, 93-100.
62. Singh, G.B., Kramer, J.A. and Krawetz, S.A. (1997) Mathematical model to predict regions of chromatic attachment to the nuclear matrix. Nucl. Acids Res. 25, 1419-1425.
63. Slatter, R.E., Dupree, P. and Gray, J.C. (1991) A scaffold-associated DNA region is located downstream of the pea plastocyanin gene. Plant Cell, 3, 1239-1250.
64. Spiker, S. and Thompson, W.F. (1996) Nuclear matrix attachment regions and transgene expression in plants. Plant Physiol. 110, 15-21.
65. Stein, G.S., Lian, J.B., Dworetzky, S.I., Owen, T.A., Bortell, R., Bidwell, J.P. and van Wijnen, A.J. (1991) Regulation of transcription factor activity during growth and differentiation. Involvement of the nuclear matrix in concentration and localization of promoter binding proteins. J. Cell. Biochem. 47, 300-305.
66. Tikhonov, A.P., Bennetzen, J.L. and Avramova, Z.V. (2000) Structural domains and matrix attachment regions along colinear chromosomal segments of maize and sorghum. Plant Cell, 12, 249-264.
67. Travers, A.A. (1990) Why bend DNA? Cell, 60, 177-180.
68. Tsutsui, K., Tsutsui, K., Okada, S., Watarai, S., Seki, S., Yasuda, R. and Shohmori, T. (1993) Identification and characterization of a nuclear scaffold protein that binds the matrix attachment region DNA. J. Biol. Chem. 268, 12886-12894.
69. Ülker, B., Allen, G.C., Thompson, W.F., Spiker, S. and Weissinger, A.K. (1999) A tobacco matrix attachment region reduces the loss of transgene expression in the progeny of transgenic tobacco plants. Plant J. 18, 253-263.
70. Vain, P., Worland, B., Kohli, A., Snape, J.W., Christou, P., Allen, G.C. and Thompson, W.F. (1999) Matrix attachment regions increase transgene expression levels and stability in transgenic rice plants and their progeny. Plant J. 18, 233-242.
71. Vaucheret, H., Elmayan, T., Thierry, D., van der Geest, A., Hall, T., Conner, A.J., Mlynarova, L. and Nap, J.-P. (1998) Flank matrix attachment regions (MARs) from chicken, bean, yeast or tobacco do not prevent homology-dependent trans-silencing in transgenic tobacco plants. Mol. Gen. Genet. 259, 388-392.
72. Wolffe, A.P. (1994) The transcription of chromatin templates. Curr. Opin. Genet. Dev. 4, 245-254.
73. Zhao, K., Hart, C.M. and Laemmli, U.K. (1995) Visualization of chromosomal domains with boundary element-associated factor BEAF-32. Cell, 81, 879-889.
74. Zhao, K., Kas, E., Gonzalez, E. and Laemmli, U.K. (1993) SAR-dependent mobilization of histone H1 by HMG-I/Y in vitro: HMG-I/Y is enriched in H1-depleted chromatin. EMBO J. 12, 3237-3247.