Suppression of transgene silencing by matrix attachment regions in maize: A dual role for the maize 5′ ADH1 matrix attachment region

Plant Cell

Volumn 14, Issue 9, 2002, Pages 2251-2264

  Brouwer, Cory ^a   Bruce, Wesley ^a   Maddock, Sheila ^a   Avramova, Zoya ^a   Bowen, Ben ^a  

^a UNIVERSITY OF NEBRASKA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CROPS; DNA; ENZYMES; GENES; YEAST;

TRANSGENE EXPRESSION;

PLANT CELL CULTURE;

EMBRYOPHYTA; EUKARYOTA; ZEA MAYS;

EID: 0036743387     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.004028     Document Type: Article

References (76)

1. Allen, G.C., Hall, G.E., Jr., 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, G.E., Jr., Michalowski, S., Newman, W., Weissinger, A.K., Spiker, S., 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. Amati, B.B., and Gasser, S.M. (1988). Chromosomal ARS and CEN elements bind specifically to the yeast nuclear scaffold. Cell 54, 967-978.
4. An, C., Mitra, A., Choi, H.K., Costa, M.A., An, K., Thornburg, R.W., and Ryan, C.A. (1989). Functional analysis of the 3′ control region of the potato wound-inducible proteinase inhibitor II gene. Plant Cell 1, 115-122.
5. Ananiev, E.V., Phillips, R.L., and Rines, H.W. (1998). Complex structure of knob DNA on maize chromosome 9: Retrotransposon invasion into heterochromatin. Genetics 149, 2025-2037.
6. Armstrong, C.L., Green, C.E., and Phillips, R.L. (1991). Development and availability of germplasm with high type II culture formation response. Maize Genet. Coop. Newsl. 65, 92-93.
7. Avramova, Z. (2002). Heterochromatin in animals and in plants: Similarities and differences. Plant Physiol. 129, 40-49.
8. 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.
9. 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.
10. Avramova, Z., and Tikhonov, A. (1999). Are scs and scs' 'neutral' chromatin domain boundaries of the locus? Trends Genet. 15, 138-139.
11. Avramova, Z., Tikhonov, A., Chen, M., and Bennetzen, J.L. (1998). Matrix attachment regions and structural colinearity in the genomes of two grass species. Nucleic Acids Res. 26, 761-767.
12. Avramova, Z., Tikhonov, A., SanMiguel, P., Jin, Y.K., Liu, C., Woo, S.S., Wing, R.A., and Bennetzen, J.L. (1996). Gene identification in a complex chromosomal continuum by local genomic cross-referencing. Plant J. 10, 1163-1168.
13. 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.
14. Bittel, D.C., Shaver, J.M., Somers, D.A., and Gengenbach, B.G. (1996). Lysine accumulation in maize cell cultures transformed with a lysine-insensitive form of maize dihydrodipicolinate synthase. Theor. Appl. Genet. 90, 70-77.
15. Bode, J., Kohwi, Y., Dickinson, L., Joh, T., Klehr, D., Mielke, C., and Kohwi-Shigematsu, T. (1992). Biological significance of unwinding capability of nuclear matrix associating DNAs. Science 255, 195-197.
16. Bonifer, C., Yannoutsos, N., Krüger, G., Grosveld, F., and Sippel, A.E. (1994). Dissection of the locus control function located on the chicken lysozyme gene domain in transgenic mice. Nucleic Acids Res. 22, 4202-4210.
17. Bowen, B. (1992). Anthocyanin genes as visual markers in transformed maize tissues. In GUS Protocols: Using the GUS Gene as a Reporter of Gene Expression, S.R. Gallagher, ed (San Diego, CA: Academic Press), pp. 163-177.
18. 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.
19. Breyne, P., van Montagu, M., Depicker, N., 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.
20. Bruce, W., Folkerts, O., Garnaat, C., Crasta, O., Roth, B., and Bowen, B. (2000). Expression profiling of the maize flavonoid pathway genes controlled by estradiol-inducible transcription factors CRC and P. Plant Cell 12, 65-79.
21. Cai, H., and Levine, M. (1995). Modulation of enhancer-promoter interactions by insulators in the Drosophila embryo. Nature 376, 533-536.
22. Callis, J., Fromm, M., and Walbot, V. (1987). Introns increase gene expression in cultured maize cells. Genes Dev. 1, 1183-1200.
23. Capellades, M., et al. (1996). The maize caffeic acid O-methyltransferase gene promoter is active in transgenic tobacco and maize plant tissues. Plant Mol. Biol. 31, 307-322.
24. Chen, M., SanMiguel, P., de Olivieira, A., Woo, S.S., Zhang, H., Wing, R.A., and Bennetzen, J.L. (1997). Microcolinearity in sh2-homologous regions of the maize, rice, and sorghum genomes. Proc. Natl. Acad. Sci. USA 94, 3431-3435.
25. Chinn, A.M., and Comai, L. (1996). The heat shock cognate 80 gene of tomato is flanked by matrix attachment regions. Plant Mol. Biol. 32, 959-968.
26. Chinn, A.M., Payne, S.R., and Comai, L. (1996). Variegation and silencing of the heat shock cognate 80 gene are relieved by a bipartite downstream regulatory element. Plant J. 9, 325-339.
27. Cockell, M., and Gasser, S.M. (1999). Nuclear compartments and gene regulation. Curr. Opin. Genet. Dev. 9, 199-205.
28. Cunningham, J.M., Purucker, M.E., Jane, S.M., Safer, B., Vanin, E.F., Ney, P.A., Lowrey, C.H., and Nienhuis, A.W. (1994). 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 94, 1298-1308.
29. Dennis, E.S., Gerlach, W.L., Pryor, A.J., Bennetzen, J.L., Inglis, A., Llewellyn, D., Sachs, M.M., Ferl, R.J., and Peacock, W.J. (1984). Molecular analysis of the alcohol dehydrogenase (Adh1) gene of maize. Nucleic Acids Res. 12, 3983-4000.
30. de Wet, J.R., Wood, K.V., DeLuca, M., Helinski, D.R., and Subramani, S. (1987). Firefly luciferase gene: Structure and expression in mammalian cells. Mol. Cell. Biol. 7, 725-737.
31. Diamond, M.I., Miner, J.N., Yoshinaga, S.K., and Yamamoto, K.R. (1990). Transcription factor interactions: Selectors of positive or negative regulation from a single DNA element. Science 249, 1266-1272.
32. Dickinson, L.A., Dickinson, C.D., and Kohwi, S.T. (1997). An atypical homeodomain in SATB1 promotes specific recognition of the key structural element in a matrix attachment region. J. Biol. Chem. 272, 11463-11470.
33. Dillon, N., Trimborn, T., Strouboulis, J., Fraser, P., and Grosveld, F. (1997). The effect of distance on long-range chromatin interactions. Mol. Cell 1, 131-139.
34. Flavell, R.B. (1994). Inactivation of gene expression in plants as a consequence of specific sequence duplication. Proc. Natl. Acad. Sci. USA 91, 3490-3496.
35. Forrester, W.C., van Genderen, C., Jenuwein, T., and Grosschedl, R. (1994). Dependence of enhancer-mediated transcription of the immunoglobulin M gene on nuclear matrix attachment regions. Science 265, 1221-1225.
36. Fransz, P.F., Armstrong, S., de Jong, J.H., Parnell, L.D., van Drunen, C., Dean, C., Zabel, P., Bisseling, T., and Jones, G.H. (2000). Integrated cytogenetic map of chromosome arm 4S of A. thaliana: Structural organization of heterochromatic knob and centromere region. Cell 100, 367-376.
37. Gallie, D.R., Sleat, D.E., Watts, J.W., Turner, P.C., and Wilson, T.M. (1987). The 5′-leader sequence of tobacco mosaic virus RNA enhances the expression of foreign gene transcripts in vitro and in vivo. Nucleic Acids Res. 15, 3257-3273.
38. Gardner, R.C., Howarth, A.J., Hahn, P., Brown-Luedi, M., Shepherd, R.J., and Messing, J. (1981). The complete nucleotide sequence of an infectious clone of cauliflower mosaic virus by m13mp7 shotgun sequencing. Nucleic Acids Res. 9, 2871-2888.
39. Gasser, S.M., and Laemmli, U.K. (1987). A glimpse at chromosomal order. Trends Genet. 3, 16-22.
40. Grotewold, E., Chamberlain, M., Snook, M., Siame, B., Butler, L., Swenson, J., Maddock, S., Clair, G.S., and Bowen, B. (1998). Engineering secondary metabolism in maize cells by ectopic expression of transcription factors. Plant Cell 10, 721-740.
41. Hobbs, S.L.A., Kpodar, P., and DeLong, C.M.O. (1990). The effect of T-DNA copy number, position and methylation on reporter gene expression in tobacco transformants. Plant Mol. Biol. 15, 851-864.
42. Iglesias, V.A., et al. (1997). Molecular and cytogenetic analyses of stably and unstably expressed transgene loci in tobacco. Plant Cell 9, 1251-1264.
43. Jefferson, R.A., Kavanagh, T.A., and Bevan, M.W. (1987). GUS fusions: β-Glucuronidase as a sensitive and versatile gene fusion marker in higher plants. Eur. Mol. Biol. J. 6, 3901-3907.
44. Jenuwein, T., Forrester, W.C., Fernandez, H.L., Laible, G., Dull, M., and Grosschedl, R. (1997). Extension of chromatin accessibility by nuclear matrix attachment regions. Nature 385, 269-272.
45. Jin, Y.-K., and Bennetzen, J.L. (1994). Integration and nonrandom mutation of a plasma membrane proton Atpase gene fragment within the bs1 retroelement of maize. Plant Cell 6, 1177-1186.
46. Klein, T.M., Kornstein, L., Sanford, J.C., and Fromm, M.E. (1989). Genetic transformation of maize cells by particle bombardment. Plant Physiol. 91, 440-444.
47. Kohwi, S.T., Maass, K., and Bode, J. (1997). A thymocyte factor SATB1 suppresses transcription of stably integrated matrix-attachment region-linked reporter genes. Biochemistry 36, 12005-12010.
48. Lamond, A.I., and Earnshaw, W.C. (1998). Structure and function of the nucleus. Science 280, 547-553.
49. Liu, J., Bramblett, D., Zhu, Q., Lozano, M., Kobayashi, R., Ross, S.R., and Dudley, J.P. (1997). The matrix attachment region-binding protein SATB1 participates in negative regulation of tissue-specific gene expression. Mol. Cell. Biol. 17, 5275-5287.
50. Lu, G., and Bruce, W.B. (2000). A novel cis-acting element conferring root-preferred gene expression in maize. J. Plant Physiol. 156, 277-283.
51. Lyko, F., and Paro, R. (1999). Chromosomal elements conferring epigenetic inheritance. Bioessays 21, 824-832.
52. Matzke, A.J.M., and Matzke, M.A. (1998). Position effects and epigenetic silencing of plant transgenes. Curr. Opin. Plant Biol. 1, 142-148.
53. Mlynarova, L., Keizer, L.C.P., Stiekema, W.J., and Nap, J.P. (1996). Approaching the lower limits of transgene variability. Plant Cell 8, 1589-1599.
54. Mlynarova, 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.
55. Nabirochkin, S., Ossokina, M., and Heidmann, T. (1998). A nuclear matrix/scaffold attachment region co-localizes with the gypsy retrotransposon insulator sequence. J. Biol. Chem. 273, 2473-2479.
56. Paul, A.-L., and Ferl, R.J. (1991). In vivo footprinting reveals unique cis-elements and different modes of hypoxic induction in maize Adh1 and Adh2. Plant Cell 3, 159-168.
57. Peacock, W.J., Dennis, E.S., Rhoades, M.M., and Pryor, J. (1981). Highly repeated DNA sequence limited to knob heterochromatin in maize. Proc. Natl. Acad. Sci. USA 78, 4490-4494.
58. Phi-Van, L., and Strätling, W.H. (1996). Dissection of the ability of the chicken lysozyme gene 5′ matrix attachment region to stimulate transgene expression and to dampen position effects. Biochemistry 35, 10735-10742.
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. SanMiguel, P., Tikhonov, A., Jin, Y.-K., Motchoulskaya, N., Zakharov, D., Berhan, A., Springer, P., Edwards, K., Lee, M., Avramova, Z., and Bennetzen, J. (1996). Nested retrotransposons in the intergenic regions of the maize genome. Science 274, 766-768.
61. Scheuermann, R.H., and Chen, U. (1989). A developmental-specific factor binds to suppressor sites flanking the immunoglobulin heavy-chain enhancer. Genes Dev. 3, 1255-1266.
62. Schöffl, F., Schroder, 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.
63. Struhl, K., Stinchcomb, D.T., Scherer, S., and Davis, R.W. (1979). High-frequency transformation of yeast: Autonomous replication of hybrid DNA molecules. Proc. Natl. Acad. Sci. USA 76, 1035-1039.
64. Thompson, C.J., Movva, N.R., Tizard, R., Crameri, R., Davies, J.E., Lauwereys, M., and Botterman, J. (1987). Characterization of the herbicide-resistance gene bar from Streptomyces hygroscopicus. Eur. Mol. Biol. J. 6, 2519-2523.
65. 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.
66. Tikhonov, A.P., SanMiguel, P.J., Nakajima, Y., Gorenstein, N.M., Bennetzen, J.L., and Avramova, Z. (1999). Colinearity and its exceptions in orthologous adh regions of maize and sorghum. Proc. Natl. Acad. Sci. USA 96, 7409-7414.
67. 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, 253-264.
68. 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.
69. van der Geest, A.H.M., Hall, G.E.J., Spiker, S., and Hall, T.C. (1994), The β-phaseolin gene is flanked by matrix attachment regions. Plant J. 6, 413-423.
70. van Drunen, C.M., Oosterling, R.W., Keultjes, G.M., 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. Nucleic Acids Res. 25, 3904-3911.
71. Wakimoto, B.T. (1998). Beyond the nucleosome: Epigenetic aspects of position-effect variegation in Drosophila. Cell 93, 321-324.
72. Walker, J.C., Howard, E.A., Dennis, E.S., and Peacock, W.J. (1987). DNA sequences required for anaerobic expression of the maize alcohol dehydrogenase 1 gene. Proc. Natl. Acad. Sci. USA 84, 6624-6628.
73. Wallrath, L.L. (1998). Unfolding the mysteries of heterochromatin. Curr. Opin. Genet. Dev. 8, 147-153.
74. Walters, M.C., Fiering, S., Eidemiller, J., Magis, W., Groudine, M., and Martin, D.I. (1995). Enhancers increase the probability but not the level of gene expression. Proc. Natl. Acad. Sci. USA 92, 7125-7129.
75. Walters, M.C., Magis, W., Fiering, S., Eidemiller, J., Scalzo, D., Groudine, M., and Martin, D.I. (1996). Transcriptional enhancers act in cis to suppress position-effect variegation. Genes Dev. 10, 185-195.
76. West, A.G., Gaszner, M., and Felsenfeld, G. (2002). Insulators: Many functions, many mechanisms. Genes Dev. 16, 271-288.