Abstract
Many light-responsive promoters contain GATA motifs and a number of nuclear proteins have been defined that interact with these elements. Type-IV zinc-finger proteins have been extensively characterised in animals and fungi and are referred to as GATA factors by virtue of their affinity for promoter elements containing this sequence. We previously identified cDNA sequences representing four Arabidopsis thaliana type-IV zinc-finger proteins. Here we define the organisation and expression of GATA-1, GATA-2, GATA-3 and GATA-4 as well as DNA-binding characteristics of their encoded proteins. Transcripts from all four genes can be detected in all tissues examined suggesting that they are not developmentally regulated at the level of transcription. In vitro binding experiments with Escherichia coli-derived recombinant proteins were performed using motifs previously defined as targets for nuclear GATA-binding proteins. These studies reveal differences in DNA binding specificity of GATA-1 as compared to the other three proteins. In vivo protein-DNA interactions monitored by yeast one-hybrid assays reveal different binding characteristics as compared to those defined with E. coli-derived recombinant protein. Trans-activation of gene expression by the four Arabidopsis proteins via some, but not all, DNA elements tested indicates that the Arabidopsis proteins can form functional interactions with previously defined promoter elements containing GATA motifs. We conclude that the Arabidopsis type-IV zinc-finger proteins may represent the previously defined family of nuclear GATA-binding proteins implicated in light-responsive transcription.
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Abel, T., Michelson, A.M. and Maniatis, T. 1993. A Drosophila GATA family member that binds to ADH regulatory sequences is expressed in the developing fat-body. Development 119: 623–633.
Anderson, S.L., Teakle, G.R., Martinocatt, S.J. and Kay, S.A. 1994. Circadian clock-regulated and phytochrome-regulated transcription is conferred by a 78 bp cis-acting domain of the Arabidopsis cab2 promoter. Plant J. 6: 457–470.
Arabidopsis Genome Initiative. 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796–815.
Arguello-Astorga, G.R. and Herrera-Estrella, L.R. 1996. Ancestral multipartite units in light-responsive plant promoters have structural features correlating with specific phototransduction pathways. Plant Physiol. 112: 1151–1166.
Ballario, P., Vittorioso, P., Magrelli, A., Talora, C., Cabibbo, A. and Macino, G. 1996. White collar-1, a central regulator of blue-light responses in Neurospora, is a zinc-finger protein. EMBO J. 15: 1650–1657.
Borello, U., Ceccarelli, E. and Giuliano, G. 1993. Constitutive, light-responsive and circadian clock-responsive factors compete for the different l-box elements in plant light-regulated promoters. Plant J. 4: 611–619.
Buzby, J.S., Yamada, T. and Tobin, E.M. 1990. A light-regulated DNA-binding activity interacts with a conserved region of a Lemna gibba rbcS promoter. Plant Cell 2: 805–814.
Card, R.M. 1999. Functional analysis of a tobacco GATA factor. PhD thesis, University of Leeds, UK.
Castresana, C., Garcialuque, I., Alonso, E., Malik, V.S. and Cashmore, A.R. 1988. Both positive and negative regulatory elements mediate expression of a photo-regulated cab gene from Nicotiana plumbaginifolia. EMBO J. 7: 1929–1936.
Chae, K.S., Kim, J.H., Choi, Y.H., Han, D.M. and Jahng, K.Y. 1995. Isolation and characterization of a genomic DNA fragment complementing an NsdD mutation of Aspergillus nidulans. Mol. Cells 5: 146–150.
Chang, W.T., Newell, P.C. and Gross, J.D. 1996. Identification of the cell fate gene stalky in Dictyostelium. Cell 87: 471–481.
Coffman, J.A., Rai, R., Cunningham, T., Svetlov, V. and Cooper, T.G. 1996. Gat1p, a GATA family protein whose production is sensitive to nitrogen catabolite repression, participates in transcriptional activation of nitrogen-catabolic genes in Saccharomyces cerevisiae. Mol. Cell. Biol. 16: 847–858.
Cunningham, T.S. and Cooper, T.G. 1991. Expression of the dal80 gene, whose product is homologous to the GATA factors and is a negative regulator of multiple nitrogen catabolic genes in Saccharomyces cerevisiae, is sensitive to nitrogen catabolite repression. Mol. Cell. Biol. 11: 6205–6215.
Daniel-Vedele, F. and Caboche, M. 1993. A tobacco cDNA clone encoding a GATA-1 zinc-finger protein homologous to regulators of nitrogen-metabolism in fungi. Mol. Gen. Genet. 240: 365–373.
Dean, C., van den Elzen, P., Tamaki, S., Dunsmuir, P. and Bedbrook, J. 1985. Differential expression of the 8 genes of the petunia ribulose bisphosphate carboxylase small subunit multi-gene family. EMBO J. 4: 3055–3061.
Dingwall, C. and Laskey, R.A. 1991. Nuclear targeting sequences: a consensus? Trends Biochem. Sci. 16: 478–481.
Donald, R.G.K. and Cashmore, A.R. 1990. Mutation of either Gbox or I-box sequences profoundly affects expression from the Arabidopsis rbcS-1A promoter. EMBO J. 9: 1717–1726.
Drevet, J.R., Skeiky, Y.A.W. and Iatrou, K. 1994. GATA-type zinc-finger motif-containing sequences and chorion gene transcription factors of the silkworm Bombyx mori. J. Biol. Chem. 269: 10660–10667.
Drevet, J.R., Swevers, L. and Iatrou, K. 1995. Developmental regulation of a silkworm gene encoding multiple GATA-type transcription factors by alternative splicing. J. Mol. Biol. 246: 43–53.
Ellis, C.M. 1996. Regulation of Polyketide Gene Expression: Isolation and Function of Nitrogen Regulatory Factor NrfA from Penicillium urticae. Biological Sciences, University of Calgary, Canada.
Evans, T. and Felsenfeld, G. 1989. The erythroid-specific transcription factor Eryf1: a new finger protein. Cell 58: 877–885.
Evans, T., Reitman, M. and Felsenfeld, G. 1988. An erythrocytespecific DNA-binding factor recognizes a regulatory sequence common to all chicken globin genes. Proc. Natl. Acad. Sci. USA 85: 5976–5980.
Froeliger, E.H. and Carpenter, B.E. 1996. Nut1, a major nitrogen regulatory gene in Magnaporthe grisea, is dispensable for pathogenicity. Mol. Gen. Genet. 251: 647–656.
Fu, Y.H. and Marzluf, G.A. 1990. Nit-2, the major nitrogen regulatory gene of Neurospora crassa, encodes a protein with a putative zinc finger DNA-binding domain. Mol. Cell. Biol. 10: 1056–1065.
Gidoni, D., Brosio, P., Bondnutter, D., Bedbrook, J. and Dunsmuir, P. 1989. Novel cis-acting elements in petunia cab gene promoters. Mol. Gen. Genet. 215: 337–344.
Gilman, M. 1988. In: F. Ausubel, R. Brent, R. Kingston, D. Moore, J. Seidman, J. Smith and K. Struhl (Eds.) Current Protocols in Molecular Biology, John Wiley, New York, pp. 471–478.
Gilmartin, P.M., Sarokin, L., Memelink, J. and Chua, N.H. 1990. Molecular light switches for plant genes. Plant Cell 2: 369–378.
Gilmartin, P.M., Memelink, J., Hiratsuka, K., Kay, S.A. and Chua, N.H. 1992. Characterization of a gene encoding a DNA-binding protein with specificity for a light-responsive element. Plant Cell 4: 839–849.
Giuliano, G., Pichersky, E., Malik, V.S., Timko, M.P., Scolnik, P.A. and Cashmore, A.R. 1988. An evolutionarily conserved proteinbinding sequence upstream of a plant light-regulated gene. Proc. Natl. Acad. Sci. USA 85: 7089–7093.
Grob, U. and Stuber, K. 1987. Discrimination of phytochrome dependent light inducible from non-light inducible plant genes: prediction of a common light-responsive element (LRE) in phytochrome dependent light inducible plant genes. Nucl. Acids Res. 15: 9957–9973.
Haas, H., Angermayr, K. and Stoffler, G. 1997. Molecular analysis of a Penicillium chrysogenum GATA factor encoding gene (sreP) exhibiting significant homology to the Ustilago maydis urbs1 gene. Gene 184: 33–37.
Harrison, S.C. 1991. A structural taxonomy of DNA-binding domains. Nature 353: 715–719.
Hawkins, M.G. and McGhee, J.D. 1995. Elt-2, a 2nd GATA factor from the nematode Caenorhabditis elegans. J. Biol. Chem. 270: 14666–14671.
Hess, S.M., Stanford, D.R. and Hopper, A.K. 1994. SRD1, a Saccharomyces cerevisiae gene affecting pre-ribosomal-RNA processing contains a C-2/C-2 zinc-finger motif. Nucl. Acids Res. 22: 1265–1271.
Hoe, K.L., Won, M.S., Yoo, O.J. and Yoo, H.S. 1996. Molecular cloning of GAF-2, a Schizosaccharomyces pombe GATA factor, which has 2 zinc-finger sequences. Biochem. Mol. Biol. Int. 39: 127–135.
Hunter, T. and Karin, M. 1992. The regulation of transcription by phosphorylation. Cell 70: 375–387.
Jiang, Y.M. and Evans, T. 1996. The Xenopus GATA-4/5/6 genes are associated with cardiac specification and can regulate cardiacspecific transcription during embryogenesis. Dev. Biol. 174: 258–270.
Kamper, J.T., Kamper, U., Rogers, L.M. and Kolattukudy, P.E. 1994. Identification of regulatory elements in the cutinase promoter from Fusarium solani. J. Biol. Chem. 269: 9195–9204.
Ko, L.J. and Engel, J.D. 1993. DNA-binding specificities of the GATA transcription factor family. Mol. Cell. Biol. 13: 4011–4022.
Kudla, B., Caddick, M.X., Langdon, T., Martinezrossi, N.M., Bennett, C.F., Sibley, S., Davies, R.W. and Arst, H.N. 1990. The regulatory gene areA mediating nitrogen metabolite repression in Aspergillus nidulans: mutations affecting specificity of gene activation alter a loop residue of a putative zinc finger. EMBO J. 9: 1355–1364.
Lam, E. and Chua, N.H. 1989. ASF-2: a factor that binds to the cauliflower mosaic virus-35S promoter and a conserved GATA motif in cab promoters. Plant Cell 1: 1147–1156.
Lam, E., Kanomurakami, Y., Gilmartin, P., Niner, B. and Chua, N.H. 1990. A metal-dependent DNA-binding protein interacts with a constitutive element of a light-responsive promoter. Plant Cell 2: 857–866.
Laverriere, A.C., Macneill, C., Mueller, C., Poelmann, R.E., Burch, J.B.E. and Evans, T. 1994. GATA-4/5/6, a subfamily of 3 transcription factors transcribed in developing heart and gut. J. Biol. Chem. 269: 23177–23184.
Li, D. and Kolattukudy, P.E. 1995. Cloning and expression of cDNA-encoding a protein that binds a palindromic promoter element essential for induction of fungal cutinase by plant cutin. J. Biol. Chem. 270: 11753–11756.
Lin, W.H., Huang, L.H., Yeh, J.Y., Hoheisel, J., Lehrach, H., Sun, Y.H. and Tsai, S.F. 1995. Expression of a Drosophila GATA transcription factor in multiple tissues in the developing embryos: identification of homozygous lethal mutants with Pelement insertion at the promoter region. J. Biol. Chem. 270: 25150–25158.
Linden, H. and Macino, G. 1997. White collar 2, a partner in blue-light signal transduction, controlling expression of lightregulated genes in Neurospora crassa. EMBO J. 16: 98–109.
Lowry, J.A. and Atchley, W.R. 2000. Molecular evolution of the GATA family of transcription factors: conservation within the DNA-binding domain. J. Mol. Evol. 50: 103–115.
Manzara, T. and Gruissem, W. 1988. Organization and expression of the genes encoding ribulose-1,5-bisphosphate carboxylase in higher plants. Photosynth. Res. 16: 117–139.
Martin, D.I.K., Tsai, S.F. and Orkin, S.H. 1989. Increased ?-globin expression in a nondeletion HPFH mediated by an erythroidspecific DNA-binding factor. Nature 338: 435–438.
McCarthy, J.E.G. 1998. Posttranscriptional control of gene expression in yeast. Microbiol. Mol. Biol. Reviews 62: 1492–1553.
Merika, M. and Orkin, S.H. 1993. DNA-binding specificity of GATA family transcription factors. Mol. Cell. Biol. 13: 3999–4010.
Minehart, P.L. and Magasanik, B. 1991. Sequence and expression of GLN3, a positive nitrogen regulatory gene of Saccharomyces cerevisiae encoding a protein with a putative zinc finger DNAbinding domain. Mol. Cell. Biol. 11: 6216–6228.
Morrisey, E.E., Ip, H.S., Lu, M.M., Parmacek, M.S. 1996. GATA-6-a zinc-finger transcription factor that is expressed in multiple cell lineages derived from lateral mesoderm. Dev. Biol. 177: 309–322.
Nishii, A., Takemura, M., Fujita, H., Shikata, M., Yokota, A. and Kohchi, T. 1999. Characterization of a novel gene coding a putative single zinc-finger protein, ZIM, expressed during the reproductive phase in Arabidopsis thaliana. DDBJ/EMBL/GenBank databases, accession number AB035310.
Orkin, S.H. 1992. GATA-binding transcription factors in hematopoietic cells. Blood 80: 575–581.
Perisic, O. and Lam, E. 1992. A tobacco DNA-binding protein that interacts with a light-responsive box-II element. Plant Cell 4: 831–838.
Puente, P., Wei, N. and Deng, X.W. 1996. Combinatorial interplay of promoter elements constitutes the minimal determinants for light and developmental control of gene expression in Arabidopsis. EMBO J. 15: 3732–3743.
Ramain, P., Heitzler, P., Haenlin, M. and Simpson, P. 1993. Pannier, a negative regulator of achaete and scute in Drosophila, encodes a zinc-finger protein with homology to the vertebrate transcription factor GATA-1. Development 119: 1277–1291.
Sambrook, J., Fritsch, E. and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Plainview, NY.
Sarokin, L.P. and Chua, N.H. 1992. Binding-sites for 2 novel phosphoproteins, 3AF5 and 3AF3, are required for rbcS-3A expression. Plant Cell 4: 473–483.
Schiestl, R.H., Dominska, M., Petes, T.D. 1993. Transformation of Saccharomyces cerevisiae with non-homologous DNA-illegitimate integration of transforming DNA into yeast chromosomes and in vivo ligation of transforming DNA to mitochondrial DNA sequences. Mol. Cell. Biol. 13: 2697–2705.
Schindler, U. and Cashmore, A.R. 1990. Photoregulated geneexpression may involve ubiquitous DNA-binding proteins. EMBO J. 9: 3415–3427.
Simon, M.C. 1995. Gotta have GATA. Nature Genet. 11: 9–11.
Spieth, J., Shim, Y.H., Lea, K., Conrad, R. and Blumenthal, T. 1991. Elt-1, an embryonically expressed Caenorhabditis elegans gene homologous to the GATA transcription factor family. Mol. Cell. Biol. 11: 4651–4659.
Teakle, G.R. and Gilmartin, P.M. 1998. Two forms of type IV zinc-finger motif and their kingdom: specific distribution between the flora, fauna and fungi. Trends Biochem. Sci. 23: 100–102.
Teakle, G.R. and Kay, S.A. 1995. The GATA-binding protein CGF-1 is closely related to GT-1. Plant Mol. Biol. 29: 1253–1266.
Tsai, S.F., Martin, D.I.K., Zon, L.I., Dandrea, A.D., Wong, G.G. and Orkin, S.H. 1989. Cloning of cDNA for the major DNAbinding protein of the erythroid lineage through expression in mammalian cells. Nature 339: 446–451.
Voisard, C., Wang, J., McEvoy, J.L., Xu, P.L. and Leong, S.A. 1993. Urbs1, a gene regulating siderophore biosynthesis in Ustilago maydis, encodes a protein similar to the erythroid transcription factor GATA-1. Mol. Cell. Biol. 13: 7091–7100.
Voytas, D.F., Konieczny, A., Cummings, M.P. and Ausubel, F.M. 1990. The structure, distribution and evolution of the TA1 retrotransposable element family of Arabidopsis thaliana. Genetics 126: 713–721.
Weiss, M.J. and Orkin, S.H. 1995. GATA transcription factors: key regulators of hematopoiesis. Exp. Hematol. 23: 99–107.
Whyatt, D.J., Deboer, E. and Grosveld, F. 1993. The 2 zinc finger-like domains of GATA-1 have different DNA-binding specificities. EMBO J. 12: 4993–5005.
Yamamoto, M., Ko, L.J., Leonard, M.W., Beug, H., Orkin, S.H. and Engel, J.D. 1990. Activity and tissue-specific expression of the transcription factor NF-E1 multigene family. Genes Dev. 4: 1650–1662.
Zon, L.I., Mather, C., Burgess, S., Bolce, M.E., Harland, R.M. and Orkin, S.H. 1991. Expression of GATA-binding proteins during embryonic-development in Xenopus laevis. Proc. Natl. Acad. Sci. USA 88: 10642–10646.
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Teakle, G.R., Manfield, I.W., Graham, J.F. et al. Arabidopsis thaliana GATA factors: organisation, expression and DNA-binding characteristics. Plant Mol Biol 50, 43–56 (2002). https://doi.org/10.1023/A:1016062325584
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DOI: https://doi.org/10.1023/A:1016062325584