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Powerful effect of an atypical bifactorial endosperm box from wheat HMWG-Dx5 promoter in maize endosperm

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Abstract

The proximal region of the high-molecular-weight glutenin promoter of the Dx5 gene (PrHMWG-Dx5) carries an atypical bifactorial endosperm box containing two cis-acting elements, namely a G-box like motif followed by a prolamin-box motif (Pb1). Transient expression assays in maize endosperm indicate that a promoter fragment containing at least the G-box like element is necessary and sufficient for maximal expression of the HMWG-Dx5 promoter. In transformed maize, we have shown that a 89 bp sequence bearing the bifactorial endosperm box behaves like a functional cis-acting unit. Its repetition in tandem confers a strong specific additive effect specifically in endosperm tissue. In contrast, the fusion of the activation sequences 1 (as-1) and 2 (as-2) of the cauliflower mosaic virus (CaMV) 35S promoter with HMWG-Dx5 derived promoter sequences deregulates its activity in transformed maize. By gel mobility shift assays we have demonstrated that the G-box like motif may alternatively bind two protein groups which have the same DNA-binding affinities as the transcription factors of either the Opaque2 (O2) family and/or the ASF-1 family.

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References

  • Albani, D., Hammond-Kosack, M.C.U., Smith, C., Conlan, S., Colot, V., Holdsworth, M.J. and Bevan, M.W. 1997. The wheat transcriptional activator SPA: a seed-specific bZIP protein that recognizes the GCN4-like motif in the bifactorial endosperm box of prolamin genes. Plant Cell 9: 171–184.

    Google Scholar 

  • Anderson, O.D. and Greene, F.C. 1989. The characterization and comparative analysis of high-Mr glutenin genes from genomes A and B of a hexaploid bread wheat. Theor. Appl. Genet. 77: 689–700.

    Google Scholar 

  • Anderson, O.D., Greene, F.C., Yip, R.E., Halford, N.G., Shewry, P.R. and Malpica-Romero, J.-M. 1989. Nucleotide sequences of the two high-molecular-weight glutenin genes from the Dgenome of a hexaploid bread wheat, Triticum aestivum L. cv. Cheyenne. Nucl. Acids Res. 17: 461–462.

    Google Scholar 

  • Anderson, O.D., Abraham-Pierce, F.A. and Tam, A. 1998. Conservation in wheat high-molecular-weight glutenin gene promoter sequences: comparisons among loci and among alleles of the GLU-B1-1 locus. Theor. Appl. Genet. 96: 568–576.

    Google Scholar 

  • Bartels, D. and Tompson, R.D. 1986. Synthesis of mRNAs coding for abundant endosperm proteins during wheat grain development. Plant Sci. 46: 117–125.

    Google Scholar 

  • Brandt, A., Montembault, A., Cameron-Mills, V. and Rasmusen, S.K. 1985. Primary stucture of a B1 hordein gene from barley. Carlsberg Res. Commun. 50: 333–345.

    Google Scholar 

  • Chen, W., Chao, G. and Singh, K.B. 1996. The promoter of a H2O2-inducible, Arabidopsis glutathione S-transferase gene contains closely linked OBF-and OBP1-binding sites. Plant J. 10: 955–966.

    Google Scholar 

  • Cord-Neto, G., Yunes, J.A., da Silva, M.J., Vettore, A.L., Arruda, P. and Leite, A. 1995. The involvement of Opaque-2 in ?-prolamin gene regulation in maize and Coix suggests a more general role for this transcriptional activator. Plant Mol. Biol. 27: 1015–1029.

    Google Scholar 

  • Entwistle, J., Knudsen, S., Müller, M. and Cameron-Mills, V. 1991. Amber codon suppression: the in vivo and in vitro analysis of two C-hordein genes from barley. Plant Mol. Biol. 17: 1217–1231.

    Google Scholar 

  • Foley, R.C., Grossman, C., Ellis, J.G., Llewellyn, D.J., Dennis, E.S., Peacock, W.J. and Singh, K.B. 1993. Isolation of a maize bZIP protein subfamily: candidates for the ocs-element transcription factor. Plant J. 3: 669–679.

    Google Scholar 

  • Forde, B.G., Heyworth, A., Pywell, J. and Kreis, M. 1985. Nucleotide sequence of a B1 hordein gene and the identification of possible upstream regulatory elements in endosperm storageprotein genes from barley, wheat and maize. Nucl. Acids Res. 13: 7327–7339.

    Google Scholar 

  • Gaffney, T., Friedrich, L., Vernooij, B., Negrotto, D., Nye, G., Uknes, S., Ward, E., Kessmann, H. and Ryals, J. 1993. Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261: 754–756.

    Google Scholar 

  • Hammond-Kosack, M.C.U., Holdsworth, M.J. and Bevan, M.W. 1993. In vivo footprinting of a low molecular weight glutenin gene (LMWG-1D1) in wheat endosperm. EMBO J. 12: 545–554.

    Google Scholar 

  • Hill, D.E., Hope, I.A., Macke, J.P. and Struhl, K. 1986. Saturation mutagenesis of the yeast his3 regulatory site: requirements for transcriptional induction and for binding by GCN4 activator protein. Science 234: 451–457.

    Google Scholar 

  • Holdsworth, M.J., Munoz-Blanco, J., Hammond-Kosack, M., Colot, V., Schuch, W. and Bevan, M.W. 1995. The maize transcription factor Opaque-2 activates a wheat glutenin promoter in plant and yeast cells. Plant Mol. Biol. 29: 711–720.

    Google Scholar 

  • Hull, G.A., Halford, N.G., Kreis, M. and Shewry, P.R. 1991. Isolation and characterization of genes encoding rye prolamins containing a highly repetitive sequence motif. Plant Mol. Biol. 17: 1111–1115.

    Google Scholar 

  • Ishida, Y., Saito, H., Ohta, S., Hiei, Y., Komari, T. and Kumashiro, T. 1996. High efficiency transformation of maize (Zea mays L.) mediated by Agrobacterium tumefaciens. Nature Biotechnol. 14: 745–750.

    Google Scholar 

  • Jefferson, R.A., Kavanagh, T.A. and Bevan, M.W. 1987. GUS fusions: ?-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6: 3901–3907.

    Google Scholar 

  • Katagiri, F., Lam, E. and Chua, N.-H. 1989. Two tobacco DNAbinding proteins with homology to the nuclear factor CREB. Nature 340: 727–730.

    Google Scholar 

  • Kikker R.J. 1993. The Biolistic PDS-1000/He device. Plant Cell Tissue Organ Cult. 33: 221–226.

    Google Scholar 

  • Kodrzycki, R., Boston, R.S. and Larkins, B.A. 1989. The Opaque-2 mutation of maize differentially reduces zein gene transcription. Plant Cell 1: 105–114.

    Google Scholar 

  • Kreis, M., Forde, B.G., Rahman, S., Miflin, B.J. and Shewry, P.R. 1985. Molecular evolution of the seed storage proteins of barley, rye and wheat. J. Mol. Biol. 183: 499–502.

    Google Scholar 

  • 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.

    Google Scholar 

  • Lam, E., Benfey, P.N. and Chua, N.-H. 1989a. Characterization of ASF-1: a factor binding site on the 35S promoter of cauliflower mosaic virus. In: C. Lamb and R. Beachy (Eds.) Plant Gene Transfer: UCLA Symposia on Molecular and Cellular Biology, New Series, Academic Press, New York.

    Google Scholar 

  • Lam, E., Benfey, P.N., Gilmartin, P.M., Fang, R.X. and Chua, N.-H. 1989b. Site-specific mutations alter in vitro factor binding and change promoter expression pattern in transgenic plants. Proc. Natl. Acad. Sci. USA 86: 7890–7894.

    Google Scholar 

  • Lohmer, S., Maddaloni, M., Motto, M., Fonzo, N.D., Hartings, H., Salamini, F. and Thompson, R.D. 1991. The maize regulatory locus Opaque-2 encodes a DNA binding protein which activates the transcription of the b-32 gene. EMBO J. 10: 617–624.

    Google Scholar 

  • Marks, M.D., Lindell, J.S. and Larkins, B.A. 1985. Quantitative analysis of the accumulation of zein mRNA during maize endosperm development. J. Biol. Chem. 260: 16445–16450.

    Google Scholar 

  • Marzábal, P., Busk, P.K., Ludevid, M.D. and Torrent, M. 1998. The bifactorial endosperm box of ?-zein gene: characterisation and function of the Pb3 and GZM cis-acting elements. Plant J. 16: 41–52.

    Google Scholar 

  • Meshi, T. and Iwabuchi, M. 1995. Plant transcription factors. Plant Cell Physiol. 36: 1405–1420.

    Google Scholar 

  • Müller, M. and Knudsen, S. 1993. The nitrogen response of a barley C-hordein promoter is controlled by positive and negative regulation of the GCN4 and endosperm box. Plant J. 4: 343–355.

    Google Scholar 

  • Müller, M., Muth, J.R., Gallusci, P., Knudsen, S., Maddaloni, M., Motto, M., Schmitz, D., Sorensen, M.B., Salamini, F., von Wettstein, D. and Thompson, R.D. 1995. Regulation of storage protein synthesis in cereal seeds: developmental and nutritional aspects. J. Plant Physiol. 145: 606–613.

    Google Scholar 

  • Piette, J., Hirai, S. and Yaniv, M. 1988. Constitutive synthesis of activator protein 1 transcription factor after viral transformation of mouse fibroblasts. Proc. Natl. Acad. Sci. USA 85: 3401–3405.

    Google Scholar 

  • Pysh, L.D., Aukerman, M.J. and Schmidt, R.J. 1993. OHP1: a maize basic domain/leucine zipper protein that interacts with Opaque 2. Plant Cell 5: 227–236.

    Google Scholar 

  • Qin, X.-F., Holuigue, L., Horvath, D.M. and Chua, N.-H. 1994. Immediate early transcription activation by salicilic acid via the cauliflower mosaic virus as-1 element. Plant Cell 6: 863–874.

    Google Scholar 

  • Robert, L.S., Thompson, R.D. and Flavell, R.B. 1989. Tissue-specific expression of a wheat high molecular weight glutenin gene in transgenic tobacco. Plant Cell 1: 569–578.

    Google Scholar 

  • Schindler, U., Beckmann, H. and Cashmore, A.R. 1992. TGA1 and G-box binding factors: two distinct classes of Arabidopsis leucine zipper proteins compete for the G-box-like element TGACGTGG. Plant Cell 4: 1309–1319.

    Google Scholar 

  • Schmidt, R.J., Burr, F.A., Aukerman, M.J. and Burr, B. 1990. Maize regulatory gene opaque-2 encodes a protein with a leucine-zipper motif that binds to zein DNA. Proc. Natl. Acad. Sci. USA 87: 46–50.

    Google Scholar 

  • Schmidt, R.J., Ketudat, M., Aukerman, M.J. and Hoschek, G. 1992. Opaque-2 is a transcriptional activator that recognizes a specific target site in 22-KD zein genes. Plant Cell 4: 689–700.

    Google Scholar 

  • Singh, K.B. 1998. Transcriptional regulation in plants: the importance of combinatorial control. Plant Physiol. 118: 1111–1120.

    Google Scholar 

  • Singh, K.B., Tokuhisa, J.G., Dennis, E.S. and Peacock, W.J. 1989. Saturation mutagenesis of the octopine synthase enhancer: correlation of mutant phenotypes with binding of a nuclear protein factor. Proc. Natl. Acad. Sci. USA 86: 3733–3737.

    Google Scholar 

  • Sumner-Smith, M., Rafalski, J.A., Sugiyama, T., Stoll, M. and Söll, D. 1985. Conservation and variability of wheat ?/?-gliadin genes. Nucl. Acids Res. 13: 2905–2916.

    Google Scholar 

  • Takaiwa, F., Yamanouchi, U., Yoshihara, T., Washida, H., Tanabe, F., Kato, A. and Yamada, K. 1996. Characterization of common cis-regulatory elements responsible for the endosperm-specific expression of members of the rice glutelin multigene family. Plant Mol. Biol. 30: 1207–1221.

    Google Scholar 

  • Thomas, M.S. and Flavell, R.B. 1990. Identification of an enhancer element for the endosperm-specific expression of high molecular weight glutenin. Plant Cell. 2: 1171–1180.

    Google Scholar 

  • Tokuhisa, J.G., Singh, K., Dennis, E.S. and Peacock, W.J. 1990. A DNA-binding protein factor recognizes two binding domains within the octopine synthase enhancer element. Plant Cell 2: 215–224.

    Google Scholar 

  • Torrent, M., Alvarez, I., Geli, M.I., Dalcol, I. and Ludevid, D. 1997. Lysine-rich modified ?-zein accumulate in protein bodies of transiently transformed maize endosperms. Plant Mol. Biol. 34: 139–149.

    Google Scholar 

  • Vancanneyt, G., Schmidt, R., O'Connor-Sanchez, A., Willmitzer, L. and Rocha-Sosa, M. 1990. Construction of an intron-containing marker gene: splicing of the intron in transgenic plants and its use in monitoring early events in Agrobacterium-mediated plant transformation. Mol. Gen. Genet. 220: 245–250.

    Google Scholar 

  • Vicente-Carbajosa, J., Moose, S.P., Parson, R.L. and Schmidt, R.J. 1997. A maize zinc-finger protein binds the prolamin box in zein gene promoters and interacts with the basic leucine zipper transcriptional activator Opaque-2. Proc. Natl. Acad. Sci. USA 94: 7685–7690.

    Google Scholar 

  • Vicente-Carbajosa, J., Onate, L., Lara, P., Diaz, I. and Carbonero, P. 1998. Barley BLZ1: a bZIP transcriptional activator that interacts with endosperm-specific gene promoters. Plant J. 13: 629–640.

    Google Scholar 

  • Washida, H., Wu, C.-Y., Suzuki, A., Yamanouchi, U., Akihama, T., Harada, K. and Takaiwa, F. 1999. Identification of cis-regulatory elements required for endosperm expression of the rice storage protein glutelin gene Glub-1. Plant Mol. Biol. 40: 1–12.

    Google Scholar 

  • Weiher, H., Konig, M. and Gruss, P. 1983. Multiple point mutations affecting the simian virus 40 enhancer. Science 219: 626–631.

    Google Scholar 

  • Wu, C.-Y., Suzuky, A., Washida, H. and Takaiwa, F. 1998. The GCN4 motif in a rice glutelin gene is essential for endospermspecific gene expression and is activated by Opaque-2 in transgenic plant rice. Plant J. 14: 673–684.

    Google Scholar 

  • Wu, C.-Y., Washida, H., Onodera, Y., Harada, K. and Takaiwa, F. 2000. Quantitative nature of the prolamin-box, ACGT and AACA motifs in a rice glutelin gene promoter: minimal ciselement requirements for endosperm-specific gene expression. Plant J. 23: 415–421.

    Google Scholar 

  • Wurch, T., Lestienne, F. and Pauwels, P.J. 1998. A modified overlap extension PCR method to create chimeric genes in the absence of restriction enzymes. Biotechnol. Tech. 12: 653–657.

    Google Scholar 

  • Yoshihara, T., Washida, H. and Takaiwa, F. 1996. A 45-bp proximal region containing AACA and GCN4 motif is sufficient to confer endosperm-specific expression of the rice storage protein glutelin gene, GluA-3. FEBS Lett. 383: 213–218.

    Google Scholar 

  • Zhang, B., Chen,W., Foley, R.C., Buttner, M. and Singh, K.B. 1995. Interactions between distinct types of DNA binding proteins enhance binding to ocs element promoter sequences. Plant Cell 7: 2241–2252.

    Google Scholar 

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Norre, F., Peyrot, C., Garcia, C. et al. Powerful effect of an atypical bifactorial endosperm box from wheat HMWG-Dx5 promoter in maize endosperm. Plant Mol Biol 50, 699–712 (2002). https://doi.org/10.1023/A:1019953914467

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