The GA octodinucleotide repeat binding factor BBR participates in the transcriptional regulation of the homeobox gene Bkn3

Plant Journal

Volumn 34, Issue 6, 2003, Pages 813-826

  Santi, Luca ^a   Wang, Yamei ^a   Stile, Maria Rosaria ^b   Berendzen, Kenneth ^a   Wanke, Dierk ^a   Roig, Cristina ^a   Pozzi, Carlo ^c   Müller, Kai ^d   Müller, Judith ^a   Rohde, Wolfgang ^a   Salamini, Francesco ^a  

^a MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

^d RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

(GA)8; BBR; Homeobox genes; Intron mediated regulation; Knox; PRE like DNA elements

Indexed keywords

GENES; TISSUE; VIRUSES;

PROMOTER SEQUENCES;

PLANTS (BOTANY);

AMINO ACID SEQUENCE; COMPUTATIONAL BIOLOGY; DNA-BINDING PROTEINS; ENHANCER ELEMENTS (GENETICS); GENE EXPRESSION REGULATION, PLANT; GENES, HOMEOBOX; GENES, PLANT; HORDEUM; INTRONS; MOLECULAR SEQUENCE DATA; NUCLEAR LOCALIZATION SIGNALS; PLANT PROTEINS; PROMOTER REGIONS (GENETICS); REPETITIVE SEQUENCES, NUCLEIC ACID; SEQUENCE HOMOLOGY, AMINO ACID; TOBACCO; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION, GENETIC; YEASTS;

ARABIDOPSIS; BRASSICA OLERACEA VAR. BOTRYTIS; CAULIFLOWER MOSAIC VIRUS; EMBRYOPHYTA; HORDEUM VULGARE SUBSP. VULGARE; NICOTIANA TABACUM;

EID: 0038079842     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-313X.2003.01767.x     Document Type: Article

References (81)

1. Alvarez-Venegas, R. and Avramova, Z. (2001) Two Arabidopsis homologs of the animal trithorax genes: a new structural domain is a signature feature of the trithorax gene family. Gene, 271, 215-221.
2. Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A. and Struhl, K. (1994) Current Protocols in Molecular Biology. New York, USA: Wiley and Sons.
3. Badr, A., Müller, K., Schafer-Pregl, R., El Rabey, H., Effgen, S., Ibrahim, H.H., Pozzi, C., Rohde, W. and Salamini, F. (2000) On the origin and domestication history of Barley (Hordeum vulgare). Mol. Biol. Evol. 17, 499-510.
4. Bellaoui, M., Pidkowich, M.S., Samach, A., Kushalappa, K., Kohalmi, S.E., Modrusan, Z., Crosby, W.L. and Haughn, G.W. (2001) The Arabidopsis BELL1 and KNOX TALE homeodomain proteins interact through a domain conserved between plants and animals. Plant Cell, 13, 2455-2470.
5. Benton, W.D. and Davis, R.W. (1977) Screening lambda gt recombinant clones by hybridization to single plaques in situ. Science, 196, 180-182.
6. Bhat, K.M., Farkas, G., Karch, F., Gyurkovics, H., Gausz, J. and Schedl, P. (1996) The GAGA factor is required in the early Drosophila embryo not only for transcriptional regulation but also for nuclear division. Development, 122, 1113-1124.
7. Biggin, M.D. and Tjian, R. (1988) Transcription factors that activate the Ultrabithorax promoter in developmentally staged extracts. Cell, 53, 699-711.
8. 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.
9. Bradley, D., Carpenter, R., Sommer, H., Hartley, N. and Coen, E. (1993) Complementary floral homeotic phenotypes result from opposite orientations of a transposon at the plena locus of Antirrhinum. Cell, 72, 85-95.
10. Busturia, A., Lloyd, A., Bejarano, F., Zavortink, M., Xin, H. and Sakonju, S. (2001) The MCP silencer of the Drosophila Abd-B gene requires both Pleiohomeotic and GAGA factor for the maintenance of repression. Development, 128, 2163-2173.
11. Castiglioni, P., Pozzi, C., Heun, M., Terzi, V., Müller, K.J., Rohde, W. and Salamini, F. (1998) An AFLP-based procedure for the efficient mapping of mutations and DNA probes in barley. Genetics, 149, 2039-2056.
12. Chan, C.S., Rastelli, L. and Pirrotta, V. (1994) A Polycomb response element in the Ubx gene that determines an epigenetically inherited state of repression. EMBO J. 13, 2553-2564.
13. Chan, R.L., Gago, G.M., Palena, C.M. and Gonzalez, D.H. (1998) Homeoboxes in plant development. Biochim. Biophys. Acta, 1442, 1-19.
14. Chelsky, D., Ralph, R. and Jonak, G. (1989) Sequence requirements for synthetic peptide-mediated translocation to the nucleus. Mol. Cell. Biol. 9, 2487-2492.
15. Chuck, G., Lincoln, C. and Hake, S. (1996) KNAT1 induces lobed leaves with ectopic meristem when overexpressed in Arabidopsis. Plant Cell, 8, 1277-1289.
16. Clancy, M., Vasil, V., Hannah, L.C. and Vasil, I.K. (1994) Maize Shrunken-1 intron and exons regions increase gene expression in maize protoplast. Plant Sci. 98, 151-161.
17. Fang, R.X., Nagy, F., Sivasubramaniam, S. and Chua, N.H. (1989) Multiple cis regulatory elements for maximal expression of the cauliflower mosaic virus 35S promoter in transgenic plants. Plant Cell, 1, 141-150.
18. Farkas, G., Gausz, J., Galloni, M., Reuter, G., Gyurkovics, H. and Karch, F. (1994) The trithorax-like gene encodes the Drosophila GAGA factor. Nature, 371, 806-808.
19. Fridman, E., Pleban, T. and Zamir, D. (2000) A recombination hotspot delimits a wild-species quantitative trait locus for tomato sugar content to 484 bp within an invertase gene. Proc. Natl. Acad. Sci. USA, 97, 4718-4723.
20. Frisch, D.A., Harris-Haller, L.W., Yokubaitis, N.T., Thomas, T.L., Hardin, S.H. and Hall, T.C. (1995) Complete sequence of the binary vector Bin 19. Plant. Mol. Biol. 27, 405-409.
21. Gidekel, M., Jimenez, B. and Herrera-Estrella, L. (1996) The first intron of the Arabidopsis thaliana gene coding for elongation factor 1 β contains an enhancer-like element. Gene, 170, 201-206.
22. Gilmour, D.S., Thomas, G.H. and Elgin, S.C. (1989) Drosophila nuclear proteins bind to regions of alternating C and T residues in gene promoters. Science, 245, 1487-1490.
23. Goodrich, J., Puangsomlee, P., Martin, M., Long, D., Meyerowitz, E.M. and Coupland, G. (1997) A Polycomb-group gene regulates homeotic gene expression in Arabidopsis. Nature, 386, 44-51.
24. Greene, B., Walko, R. and Hake, S. (1994) Mutator insertions in an intron of the maize knotted 1 gene result in dominant suppressible mutations. Genetics, 138, 1275-1285.
25. Gremke, L., Lord, P.C., Sabacan, L., Lin, S.C., Wohlwill, A. and Storti, R.V. (1993) Coordinate regulation of Drosophila tropomyosin gene expression is controlled by multiple muscle-type-specific positive and negative enhancer elements. Dev. Biol. 159, 513-527.
26. Grossniklaus, U., Vielle-Calzada, J.P., Hoeppner, M.A. and Gagliano, W.B. (1998) Maternal control of embryogenesis by MEDEA, a polycomb group gene in Arabidopsis. Science, 280, 446-450.
27. Hake, S., Vollbrecht, E. and Freeling, M. (1989) Cloning Knotted, the dominant morphological mutant in maize using Ds2 as a transposon tag. EMBO J. 8, 15-22.
28. Harlan, H.V. (1931) The origin of hooded barley. J. Hered. 22, 265-272.
29. Heun, M., Kennedy, A.E., Anderson, J.A., Lapitan, N.L., Sorrells, M.E. and Tanksley, S.D. (1991) Construction of a restriction fragment length polymorphism map for barley (Hordeum vulgare). Genome, 34, 437-447.
30. Hinz, U., Wolk, A. and Renkawitz-Pohl, R. (1992) Ultrabithorax is a regulator of beta 3 tubulin expression in the Drosophila visceral mesoderm. Development, 116, 543-554.
31. Hodgson, J.W., Argiropoulos, B. and Brock, H.W. (2001) Site-specific recognition of a 70-base-pair element containing d(GA)(n) repeats mediates bithoraxoid polycomb group response element-dependent silencing. Mol. Cell. Biol. 21, 4528-4543.
32. Hoekema, A., Hirsch, P.R., Hooykaas, P.J.J. and Schilperoort, R.A. (1983) A binary plant transformation vector strategy based upon separation of vir- and T-region of A. tumefaciens. Nature, 303, 179-180.
33. Hwang, E.S., Choi, A. and Ho, I.C. (2002) Transcriptional regulation of GATA-3 by an intronic regulatory region and fetal liver zinc finger protein 1. J. Immunol. 169, 248-253.
34. Jach, G., Binot, E., Frings, S., Luxa, K. and Schell, J. (2001) Use of red fluorescent protein from Discosoma sp. (dsRED) as a reporter for plant gene expression. Plant J. 28, 483-491.
35. Jackson, D., Veit, B. and Hake, S. (1994) Expression of maize KNOTTED1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot. Development, 120, 405-413.
36. Jefferson, R.A., Bevan, M. and Kavanagh, T. (1987) The use of the Escherichia coli beta-glucuronidase as a gene fusion marker for studies of gene expression in higher plants. Biochem. Soc. Trans. 15, 17-18.
37. Katsani, K.R., Hajibagheri, M.A. and Verrijzer, C.P. (1999) Cooperative DNA binding by GAGA transcription factor requires the conserved BTB/POZ domain and reorganizes promoter topology. EMBO J. 18, 698-708.
38. Kawalleck, P., Somssich, I.E., Feldbrugge, M., Hahlbrock, K. and Weisshaar, B. (1993) Polyubiquitin gene expression and structural properties of the ubi4-2 gene in Petroselinum crispum. Plant. Mol. Biol. 21, 673-684.
39. Kehle, J., Beuchle, D., Treuheit, S., Christen, B., Kennison, J.A., Bienz, M. and Müller, J. (1998) dMi-2, a hunchback-interacting protein that functions in polycomb repression. Science, 282, 1897-1900.
40. Kennison, J.A. (1995) The Polycomb and trithorax group proteins of Drosophila: trans- regulators of homeotic gene function. Annu. Rev. Genet. 29, 289-303.
41. Kerstetter, R.A., Laudencia-Chingcuanco, D., Smith, L.G. and Hake, S. (1997) Loss-of-function mutations in the maize homeobox gene, knotted1, are defective in shoot meristem maintenance. Development, 124, 3045-3054.
42. Koncz, C., Martini, N., Szabados, L., Hrouda, P.S., Bachmair, A. and Shell, J. (1994) Plant Molecular Biology Manual, Vol. B2 (Gevin, S.B. and Schilleport, R.A., eds). Dordrecht, the Netherlands: Kluwer, pp. 1-22.
43. Lander, E.S., Green, P., Abrahamson, J., Barlow, A., Daly, M.J., Lincoln, S.E. and Newburg, L. (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics, 1, 174-181.
44. Lehmann, M., Siegmund, T., Lintermann, K.G. and Korge, G. (1998) The Pipsqueak protein of Drosophila melanogaster binds to GAGA sequences through a novel DNA-binding domain. J. Biol. Chem. 273, 28504-28509.
45. Lin, J. and Müller, K.J. (2002) Structure and development of epiphylly in knox-transgenic tobacco. Planta, 214, 521-525.
46. Long, J.A., Moan, E.I., Medford, J.I. and Barton, M.K. (1996) A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature, 379, 66-69.
47. Luehrsen, K.R., de Wet, J.R. and Walbot, V. (1992) Transient expression analysis in plants using firefly luciferase reporter gene. Meth. Enzymol. 216, 397-414.
48. Luehrsen, K.R. and Walbot, V. (1991) Intron enhancement of gene expression and the splicing efficiency of introns in maize cells. Mol. Gen. Genet. 225, 81-93.
49. Matsuoka, M. and Sanada, Y. (1991) Expression of photosynthetic genes from the C4 plant, maize, in tobacco. Mol. Gen. Genet. 225, 411-419.
50. Müller, K.J. (1997) Die Homöboxgene der Knox-Familie in Gerste (Hordeum vulgare L.): Molekulare Characterisierung, transgene Expression und Assoziationversuche mit Homöotischen Mutationen. Dissertation. Köln: Universität zu Köln.
51. Müller, C. and Leutz, A. (2001) Chromatin remodeling in development and differentiation. Curr. Opin. Genet. Dev. 11, 167-174.
52. Müller, K.J., Romano, N., Gerstner, O., Garcia-Maroto, F., Pozzi, C., Salamini, F. and Rohde, W. (1995) The barley Hooded mutation caused by a duplication in a homeobox gene intron. Nature, 374, 727-730.
53. Müller, J., Wang, Y., Franzen, R., Santi, L., Salamini, F. and Rohde, W. (2001) In vitro interactions between barley TALE homeodomain proteins suggest a role for protein-protein associations in the regulation of Knox gene function. Plant J. 27, 13-23.
54. Nakai, K. and Kanehisa, M. (1992) A knowledge base for predicting protein localization sites in eukaryotic cells. Genomics, 14, 897-911.
55. Negrutiu, I., Shillito, R., Potrykus, I., Biasini, G. and Sala, F. (1987) Hybrid genes in the analysis of transformation conditions. Part I. setting up a simple method for direct gene transfer in plant protoplast. Plant Mol. Biol. 8, 363-373.
56. Odell, J.T., Nagy, F. and Chua, N.H. (1985) Identification of DNA sequences required for activity of the cauliflower mosaic virus 35S promoter. Nature, 313, 810-812.
57. Paro, R. and Harte, J. (1996) The role of Polycomb group and trithorax group chromatin complexes in the maintenance of determined cell states. In Epigenetics Mechanisms of Gene Regulation (Russo, V.E.A., Mactiensen, R.A. and Riggs, A., eds). Cold Spring Harbor: Cold Spring Harbor Laboratory Press, pp. 507-528.
58. Plesse, B., Criqui, M.C., Durr, A., Parmentier, Y., Fleck, J. and Genschik, P. (2001) Effects of the polyubiquitin gene Ubi U4 leader intron and first ubiquitin monomer on reporter gene expression in Nicotiana tabacum. Plant. Mol. Biol. 45, 655-667.
59. Pozzi, C., Müller, K.J., Rohde, W. and Salamini, F. (1999) Leaf development. In Development - Genetics, Epigenetics and Environmental Regulation (Russo, V.E.A., Cove, D.J., Edgar, L.G., Jaenisch, R. and Salamini, F., eds). Berlin: Springer Verlag, pp. 146-165.
60. Pozzi, C., Faccioli, P., Terzi, V. et al. (2000) Genetics of mutations affecting the development of a barley floral bract. Genetics, 154, 1335-1346.
61. Pozzi, C., Dipietro, D., Halas, G., Roig, C. and Salamini, F. (2003) Integration of a barley (H. vulgare) molecular linkage map with the position of genetic loci hosting 29 developmental mutants. Heredity, in press.
62. Robbins, J., Dilworth, S.M., Laskey, R.A. and Dingwall, C. (1991) Two interdependent basic domains in nucleoplasmin nuclear targeting sequence: identification of a class of bipartite nuclear targeting sequence. Cell, 64, 615-623.
63. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.
64. Sangwan, I. and O'Brian, M.R. (2002) Identification of a soybean protein that interacts with GAGA element dinucleotide repeat DNA. Plant Physiol. 129, 1788-1794.
65. Seul, K.H. and Beyer, E.C. (2000) Mouse connexin37: gene structure and promoter analysis. Biochim. Biophys. Acta, 1492, 499-504.
66. Shamsher, M.K., Chuzhanova, N.A., Friedman, B., Scopes, D.A., Alhaq, A., Millar, D.S., Cooper, D.N. and Berg, L.P. (2000) Identification of an intronic regulatory element in the human protein C (PROC) gene. Hum. Genet. 107, 458-465.
67. Sheen, J., Hwang, S., Niwa, Y., Kobayashi, H. and Galbraith, D.W. (1995) Green-fluorescent protein as a new vital marker in plant cells. Plant J. 8, 777-784.
68. Sieburth, L.E. and Meyerowitz, E.M. (1997) Molecular dissection of the AGAMOUS control region shows that cis elements for spatial regulation are located intragenically. Plant Cell, 9, 355-365.
69. Soeller, W.C., Oh, C.E. and Kornberg, T.B. (1993) Isolation of cDNAs encoding the Drosophila GAGA transcription factor. Mol. Cell. Biol. 13, 7961-7970.
70. Soeller, W.C., Poole, S.J. and Kornberg, T.B. (1988) In vitro transcription of the Drosophila engrailed gene. Genes Dev. 2, 68-81.
71. Sprenger-Haussels, M. and Weisshaar, B. (2000) Transactivation properties of parsley proline-rich bZIP transcription factors. Plant J. 22, 1-8.
72. Stebbins, G.L. and Yagil, E. (1966) The morphogenetic effects of the Hooded gene in barley. I. The course of development in Hooded and Awned genotypes. Genetics. 54, 727-741.
73. Strizhov, N., Keller, M., Mathur, J., Koncz-Kalman, Z., Bosch, D., Prudovsky, E., Schell, J., Sneh, B., Koncz, C. and Zilberstein, A. (1996) A synthetic crylC gene, encoding a Bacillus thuringiensis delta-endotoxin, confers Spodoptera resistance in alfalfa and tobacco. Proc. Natl. Acad. Sci. USA, 93, 15012-15017.
74. Topfer, R., Matzeit, V., Gronenborn, B., Schell, J. and Steinbiss, H.H. (1987) A set of plant expression vectors for transcriptional and translational fusions. Nucl. Acids Res. 15, 5890.
75. Tsukiyama, T., Becker, P.B. and Wu, C. (1994) ATP-dependent nucleosome disruption at a heat-shock promoter mediated by binding of GAGA transcription factor. Nature, 367, 525-532.
76. Varotto, C., Maiwald, D., Pesaresi, P., Jahns, P., Salamini, F. and Leister, D. (2002) The metal ion transporter IRT1 is necessary for iron homeostasis and efficient photosynthesis in Arabidopsis thaliana. Plant J. 31, 589-599.
77. Vollbrecht, E., Reiser, L. and Hake, S. (2000) Shoot meristem size is dependent on inbred background and presence of the maize homeobox gene Knotted1. Development, 127, 3161-3172.
78. Vollbrecht, E., Veit, B., Sinha, N. and Hake, S. (1991) The developmental gene Knotted-1 is a member of a maize homeobox gene family. Nature, 350, 241-243.
79. Wilde, R.J., Cooke, S.E., Brammar, W.J. and Schuch, W. (1994) Control of gene expression in plant cells using a 434: VP16 chimeric protein. Plant Mol. Biol. 24, 381-388.
80. Wilkins, R.C. and Lis, J.T. (1999) DNA distortion and multimerization: novel functions of the glutamine-rich domain of GAGA factor. J. Mol. Biol. 285, 515-525.
81. Yanofsky, M.F., Ma, H., Bowman, J.L., Drews, G.N., Feldmann, K.A. and Meyerowitz, E.M. (1990) The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature, 346, 35-39.