Skip to main content
Log in

Chromatin structure and phaseolin gene regulation

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Chromatin structure, the organized packaging of DNA with histones in the nucleus, is now seen as a dynamic fabric that changes with development. Here, we use studies on the phaseolin (phas) gene that encodes a seed protein to show how chromatin structure interacts with the transcription machinery to accomplish rigorous spatial regulation of expression. In leaf and other vegetative tissues, a nucleosome is rotationally and translationally positioned over an ensemble of three phased TATA boxes, denying access to TBP. Current interest focuses on the mechanisms by which this architecture is remodeled during embryogenesis. The transcription factor PvALF is intrinsically involved, as are other non-histone proteins and abscisic acid. These concepts, and the possible modular nature of phas expression, are summarized together with speculations concerning the re-establishment of the nucleosome over the phas promoter during terminal stages of embryogenesis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

REFERENCES

  • Aalfs, J.D. and Kingston, R.E. 2000. What does ‘chromatin remod-eling’ mean? Trends Biochem. Sci. 25: 548–555.

    Google Scholar 

  • Almer, A. and Horz, W. 1986. Nuclease hypersensitive regions with adjacent positioned nucleosomes mark the gene boundaries of the HPO5/PHO3 locus in yeast. EMBO J. 5: 2681–2687.

    Google Scholar 

  • Bäumlein, H., Nagy, I., Villaroel, R., Inzé, D. and Wobus, U. 1992. Cis-analysis of a seed protein gene promoter: the conservative RY repeat CATGCATG within the legumin box is essential for tissue-specific expression of a legumin gene. Plant J. 233–239.

  • Bino, R.J., Lanteri, S., Verhoeven, H.A. and Kraak, H.L. 1993. Flow cytometric determination of nuclear replication stages in seed tissues. Ann. Bot. 72: 181–187.

    Google Scholar 

  • Bobb, A.J., Chern, M.S. and Bustos, M.M. 1997. Conserved RY-repeats mediate transactivation of seed-specific promoters by the developmental regulator PvALF. Nucl. Acids Res. 25: 641–647.

    Google Scholar 

  • Bobb, A.J., Eiben, H.G. and Bustos, M.M. 1995. PvAlf, an embryo-specific acidic transcriptional activator, enhances gene expression from phaseolin and phytohemagglutinin promoters. Plant J. 8: 331–343.

    Google Scholar 

  • Busk, P.K. and Pagès, M. 1998. Regulation of abscisic acid-induced transcription. Plant Mol. Biol. 37: 425–435

    Google Scholar 

  • Bustos, M.M., Begum, D., Kalkan, F.A., Battraw, M.J. and Hall, T.C. 1991. Positive and negative cis-acting DNA domains are required for spatial and temporal regulation of gene expression by a seed storage protein promoter. EMBO J. 10: 1469–1479.

    Google Scholar 

  • Bustos, M.M., Iyer, M. and Gagliardi, S.J. 1998. Induction of a β-phaseolin promoter by exogenous abscisic acid in tobacco: de-velopmental regulation and modulation by external sucrose and Ca2+ ions. Plant Mol. Biol. 37: 265–274.

    Google Scholar 

  • Chern, M.S., Bobb, A.J. and Bustos, M.M. 1996a. The regulator of MAT2 (ROM2) protein binds to early maturation promoters and represses PvALF-activated transcription. Plant Cell 8: 305–321.

    Google Scholar 

  • Chern, M.S., Eiben, H.G. and Bustos, M.M. 1996b. The develop-mentally regulated bZIP factor ROM1 modulates transcription from lectin and storage protein genes in bean embryos. Plant J. 10: 135–148.

    Google Scholar 

  • Corke, F.M.K., Hedley, C.L. and Wang, T.L. 1990a. An analysis of seed development in Pisum sativum L. XI. Cellular development and the deposition of storage protein in immature embryos grown in vivo and in vitro. Protoplasma 155: 127–135.

    Google Scholar 

  • Corke, F.M.K., Hedley, C.L. and Wang, T.L. 1990b. An analysis of seed development in Pisum sativum L. XII. In vitro manip-ulation of embryo development using xenobiotic compounds. Protoplasma 155: 136–143.

    Google Scholar 

  • Frisch, D.A., van der Geest, A.H.M., Dias, K. and Hall, T.C. 1995. Chromosomal integration is required for spatial regulation of expression from the β-phaseolin promoter. Plant J. 7: 503–512.

    Google Scholar 

  • Goldberg, R.B., de Paiva, G. and Yadegari, R. 1994. Plant embryo-genesis: zygote to seed. Science 266: 605–614.

    Google Scholar 

  • Gomez-Cadenas, A., Verhey, S.D., Holappa, L.D., Shen, Q., Ho, T.H. and Walker-Simmons, M.K. 1999. An abscisic acid-induced protein kinase, PKABA1, mediates abscisic acid-suppressed gene expression in barley aleurone layers. Proc. Natl. Acad. Sci. USA 96: 1767–1772.

    Google Scholar 

  • Gosti, F., Beaudoin, N., Serizet, C., Webb, A.A., Vartanian, N. and Giraudat, J. 1999. ABI1 protein phosphatase 2C is a negative regulator of abscisic acid signaling. Plant Cell 11: 1897–1910.

    Google Scholar 

  • Grill, F. and Himmelbach, A. 1998. ABA signal transduction. Curr. Opin. Plant Biol. 1: 412–418.

    Google Scholar 

  • Guiltinan, M.J., Marcotte, W.R. Jr. and Quatrano, R.S. 1990. A plant leucine zipper protein that recognizes an abscisic acid response element. Science 250: 167–271.

    Google Scholar 

  • Hall, T.C., Ma, Y., Buchbinder, B.U., Pyne, J.W., Sun, S.M. and Bliss, F.A. 1978. Messenger RNA for G1 protein of French bean seeds: cell-free translation and product characterization. Proc. Natl. Acad. Sci. USA 75: 3196–3200.

    Google Scholar 

  • Hall, T.C., Li, G. and Chandrasekharan, M.B. 1998. Participation of chromatin in the regulation of phaseolin gene expression. J. Plant Physiol. 152: 614–620.

    Google Scholar 

  • Hall, T.C., Chandrasekharan, M.B. and Li, G. 1999. Phaseolin: its past, properties, regulation and future. In: P.R. Shewry and R. Casey (Eds.) Seed Proteins, Kluwer Academic Publishers, Dordrecht, Netherlands, pp. 209–240.

    Google Scholar 

  • Himmelbach, A., Iten, M. and Grill, E. 1998. Signalling of abscisic acid to regulate plant growth. Phil. Trans. R. Soc. Lond. B: Biol. Sci. 353: 1439–1444.

    Google Scholar 

  • Hobo, T., Kowyama, Y. and Hattori, T. 1999. A bZIP factor, TRAB1, interacts with VP1 and mediates abscisic acid-induced transcription. Proc. Natl. Acad. Sci. USA 96: 15348–15353.

    Google Scholar 

  • Hoecker, U., Vasil, I.K. and McCarty, D.R. 1995. Integrated con-trol of seed maturation and germination programs by activator and repressor functions of Viviparous-1 of maize. Genes Dev. 9: 2459–2469.

    Google Scholar 

  • Iyer, L.M., Kumpatla, S.P., Chandrasekharan, M.B. and Hall, T.C. 2000. Transgene silencing in monocots. Plant. Mol. Biol. 43: 323–346.

    Google Scholar 

  • Kawagoe, Y. and Murai, N. 1996. A novel basic region/helix-loop-helix protein binds to a G-box motif CACGTG of the bean seed storage protein β-phaseolin gene. Plant Sci. 116: 47–57.

    Google Scholar 

  • Kawagoe, Y., Campbell, B.R. and Murai, N. 1994. Synergism be-tween CACGTG (G-box) and CACCTG cis-elements is required for activation of the been seed storage protein β-phaseolin gene. Plant J. 5: 885–890.

    Google Scholar 

  • Larkins, B.A., Jones, R.A. and Tsai, C.Y. 1976. Isolation and in vitro translation of zein messenger ribonucleic acid. Biochemistry 15: 5506–5511.

    Google Scholar 

  • Li, G., Chandler, S.P., Wolffe, A.P. and Hall, T.C. 1998. Architec-tural specificity in chromatin structure at the TATA box in vivo: nucleosome displacement upon β-phaseolin gene activation. Proc. Natl. Acad. Sci. USA 95: 4772–4777.

    Google Scholar 

  • Li, G., Bishop, K.J., Chandrasekharan, M.B. and Hall, T.C. 1999. β-phaseolin gene activation is a two-step process: PvAlf-mediated chromatin modification followed by abscisic acid-mediated gene activation. Proc. Natl. Acad. Sci. USA 96: 7104–7109.

    Google Scholar 

  • Li, G., Bishop, K.J. and Hall, T.C. 2001. De novo activation of the β-phaseolin promoter by phosphatase or protein synthesis inhibitors. J. Biol. Chem. 276: 2062–2068.

    Google Scholar 

  • Luan, S. 1998. Protein phosphatases and signaling cascades in higher plants. Trends Plant Sci. 3: 271–275.

    Google Scholar 

  • Matzke, M.A., Mette, M.F. and Matzke, A.J. 2000. Transgene silencing by the host genome defense: implications for the evolu-tion of epigenetic control mechanisms in plants and vertebrates. Plant Mol. Biol. 43: 401–415.

    Google Scholar 

  • Mayer, U., Torres Ruiz, R.A., Berleth, T., Miséra, S. and Jürgens, G. 1991. Mutations affecting body organization in the Arabidopsis embryo. Nature 353: 402–407.

    Google Scholar 

  • Meyer, P. 2000. Transcriptional transgene silencing and chromatin components. Plant Mol. Biol. 43: 221–234.

    Google Scholar 

  • Mundy, J., Yamaguchi-Shinozaki, K. and Chua, N.-H. 1990. Nu-clear proteins bind conserved elements in the abscisic acid-responsive promoter of a rice rab gene. Proc. Natl. Acad. Sci. USA 87: 1406–1410.

    Google Scholar 

  • Murray, M.G. and Kennard, W.C. 1984. Altered chromatin con-formation of the higher plant gene phaseolin. Biochemistry 23: 4225–4232.

    Google Scholar 

  • Ogas, J., Kaufmann, S., Henderson, J. and Somerville, C. 1999. PICKLE is a CHD3 chromatin-remodeling factor that regu-lates the transition from embryonic to vegetative development in Arabidopsis. Proc. Natl. Acad. Sci. USA 96: 13839–13844.

    Google Scholar 

  • Parcy, F. and Giraudat, J. 1997. Interactions between the ABI1 and the ectopically expressed ABI3 genes in controlling abscisic acid responses in Arabidopsis vegetative tissues. Plant J. 11: 693–702.

    Google Scholar 

  • Reidt, W., Wohlfahrt, T., Ellerstrom, M., Czihal, A., Tewes, A., Ezcurra, I., Rask, L. and Bäumlein, H. 2000. Gene regulation during late embryogenesis: the RY motif of maturation-specific gene promoters is a direct target of the FUS3 gene product. Plant J. 21: 401–408.

    Google Scholar 

  • Richard-Foy, H. and Hager, G.L. 1987. Sequence-specific position-ing of nucleosomes over the steroid-inducible MMTV promoter. EMBO J. 6: 2321–2328.

    Google Scholar 

  • Sengupta-Gopalan, C., Reichert, N.A., Barker, RF., Hall, T.C., and Kemp, J.D. 1985. Developmentally regulated expression of the bean β-phaseolin gene in tobacco seed. Proc. Natl. Acad. Sci. USA 82: 3320–3324.

    Google Scholar 

  • Shimizu, M., Roth, S.Y., Szent-Gyorgyi, C. and Simpson, R.T. 1991. Nucleosomes are positioned with base pair precision adja-.129 cent to the alpha 2 operator in Saccharomyces cerevisiae.EMBO J. 10: 3033–3041.

    Google Scholar 

  • Simpson, R.T. 1991. Nucleosome positioning: occurrence, mecha-nisms, and functional consequences. Prog. Nucl. Acids Res. Mol. Biol. 40: 183–184.

    Google Scholar 

  • Straka, C. and Horz, W. 1991. A functional role for nucleosomes in the repression of a yeast promoter. EMBO J. 10: 361–368.

    Google Scholar 

  • Sun, S.M., Buchbinder, B.U. and Hall, T.C. 1975. Cell-free synthe-sis of the major storage protein of the bean, Phaseolus vulgaris L. Plant Physiol. 56: 780–785.

    Google Scholar 

  • Sun, S.M., Slightom, J.L. and Hall, T.C. 1981. Intervening se-quences in a plant gene: comparison of the partial sequence of a cDNA and genomic DNA of French bean phaseolin. Nature 289: 37–41.

    Google Scholar 

  • Sussex, I.M. and Dale, R.M.K. 1979. Hormonal control of stor-age protein synthesis in Phaseolus vulgaris. In: I. Rubenstein, R.L. Phillips, C.E. Green and B.G. Gengenbach (Eds.) The Plant Seed: Development, Preservation and Germination, Academic Press, New York, pp. 129–141.

    Google Scholar 

  • Suzuki, M. Kao, C.Y. and McCarty, D.R. 1997. The conserved B3 domain of VIVIPAROUS1 has a cooperative DNA binding activity. Plant Cell 9: 799–807.

    Google Scholar 

  • van der Geest, A.H.M., and Hall, T.C. 1996. A 68 bp element of the β-phaseolin promoter functions as a seed-specific enhancer. Plant Mol. Biol. 32: 579–588.

    Google Scholar 

  • van der Geest, A.H.M. and Hall, T.C. 1997. The β-phaseolin 5′ matrix attachment region acts as an enhancer facilitator. Plant Mol. Biol. 33: 553–557.

    Google Scholar 

  • 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.

    Google Scholar 

  • van der Geest, A.H.M., Frisch, D.A., Kemp, J.D. and Hall, T.C. 1995. Cell ablation reveals that expression from the phaseolin promoter is confined to embryogenesis and microsporogenesis. Plant Physiol. 109: 1151–1158.

    Google Scholar 

  • Wolffe, A.P. and Guschin, D. 2000. Review: chromatin structural features and targets that regulate transcription. J. Struct. Biol. 129: 102–122.

    Google Scholar 

  • Yudkovsky, N., Logie, C., Hahn, S. and Peterson, C.L. 1999. Re-cruitment of the SWI/SNF chromatin remodeling complex by transcriptional activators. Genes Dev. 13: 2369–2374.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Li, G., Chandrasekharan, M.B., Wolffe, A.P. et al. Chromatin structure and phaseolin gene regulation. Plant Mol Biol 46, 121–129 (2001). https://doi.org/10.1023/A:1010693703421

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1010693703421

Navigation