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Gibberellin-responsive genes: high level of transcript accumulation in leaf sheath meristematic tissue from Zea mays L.

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Abstract

In order to identify genes that are related to the gibberellin (GA) response in maize (Zea mays L.), mRNA species from wild-type and single-gene dwarf mutants, d5 and D8, were compared by fluorescent differential display. The d5 mutant is unable to produce biologically active GA, but recovers its tall stature on exogenous application of GA. D8 is insensitive to GA, despite the accumulation of a high level of endogenous GA, suggesting it to be a receptor mutant or a mutant in signal transduction pathway(s). After screening 7000 cDNA populations, one clone was isolated, for which transcripts were rare in d5 shoots but accumulated within 1 h after GA3 application. This clone, designated as ZmGR1a, encodes a polypeptide with a relative molecular mass of ca. 13 kDa, which shows significant homology to proline-rich proteins from several plant species. A similar experiment with D8 identified a clone, ZmGR2a, with low transcript levels, but accumulation within 6 h after GA3 treatment of d5 shoots. ZmGR2a encodes a polypeptide with a relative molecular mass of ca. 19 kDa, which shows no significant homology with any known protein. Southern blot analysis indicated that ZmGR1a and ZmGR2a form a small multigene family within the maize genome. In situ hybridization with wild-type seedlings showed transcripts on both to be abundant in leaf sheath meristematic tissue, in which GA enhances cell elongation and cell division.

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References

  • Branca, C., Ricci, D. and Bassi, M. 1988. Epidermis integrity and epicotyl growth in the azuki bean. J. Plant Growth Regul. 7: 95-109.

    Google Scholar 

  • Bush, D.S. 1995. Calcium regulation in plant cells and its role in signaling. Annu. Rev. Plant Physiol. PlantMol. Biol. 46: 95-122.

    Google Scholar 

  • Cassab, G.I. and Varner, J.E. 1988. Cell wall proteins. Annu. Rev. Plant Physiol. 39: 321-353.

    Google Scholar 

  • Chen, X.-F., Chang, M., Wang, B. and Wu, R. 1997. Cloning of Ca2C-ATPase gene and the role of cytosolic Ca2C in the gibberellin-dependent signaling pathway in aleurone cells. Plant J. 11: 363-371.

    PubMed  Google Scholar 

  • Cho, H.-T. and Kende, H. 1997. Expression of expansin genes is correlated with growth in deepwater rice. Plant Cell 9: 1661-1671.

    Google Scholar 

  • Choi, D.-W., Song, J.Y., Kwon, Y.M. and Kim, S.G. 1996. Characterization of a cDNA encoding a proline-rich 14 kDa protein in developing cortical cells of the roots of bean (Phaseolus vulgaris) seedlings. Plant Mol. Biol. 30: 973-982.

    PubMed  Google Scholar 

  • Chory, J., Voytas, D.F., Olszewski, N.E. and Ausubel, F.M. 1987. Gibberellin-induced changes in the populations of translatable mRNAs and accumulated polypeptides in dwarfs of maize and pea. Plant Physiol. 83: 15-23.

    Google Scholar 

  • Church, G.M. and Gilbert, W. 1984. Genomic sequencing. Proc. Natl. Acad. Sci. USA 81: 1991-1995.

    PubMed  Google Scholar 

  • Dingwall C. and Laskey, R.A. 1991. Nuclear targeting sequences: a consensus? Trends Biochem. Sci. 16: 478-481.

    Article  PubMed  Google Scholar 

  • Foster, C.A. 1977. Slender: an accelerated extension growth mutant in barley. Barley Genet. Newsl. 7: 24-27.

    Google Scholar 

  • Fujioka, S., Yamane, H., Spray, C.R., Gaskin, P., MacMillan, J., Phinney, B.O. and Takahashi, N. 1988a. Qualitative and quantitative analyses of gibberellins in vegetative shoots of normal, dwarf-1, dwarf-2, dwarf-3 and dwarf-5 seedlings of Zea mays L. Plant Physiol. 88: 1367-1372.

    Google Scholar 

  • Fujioka, S., Yamane, H., Spray, C.R., Katsumi, M., Phinney, B.O., Gaskin, P., MacMillan, J. and Takahashi, N. 1988b. The dominant non-gibberellin-responding dwarf mutant (D8) of maize accumulates native gibberellins. Proc. Natl. Acad. Sci. USA 85: 9031-9035.

    Google Scholar 

  • Gale, M.D. and Marshall, G.A. 1973. Insensitivity to gibberellin in dwarf wheats. Ann. Bot. 37: 729-735.

    Google Scholar 

  • Gilroy S. 1996. Signal transduction in barley aleurone protoplasts is calcium dependent and independent. Plant Cell 8: 2193-2209.

    Article  PubMed  Google Scholar 

  • Gilroy, S. and Jones, R.L. 1994. Perception of gibberellin and abscisic acid at the external face of the plasma membrane of barley (Hordeum vulgare L.) aleurone protoplasts. Plant Physiol. 104: 1185-1192.

    PubMed  Google Scholar 

  • Gubler, F., Kalla, R., Roberts, J.K. and Jacobsen, J.V. 1995. Gibberellin-regulated expression of a myb gene in barley aleurone cells: evidence for Myb transactivation of a high-pI _-amylase gene promoter. Plant Cell 7: 1879-1891.

    Article  PubMed  Google Scholar 

  • Hooley, R., Beale, M.H. and Smith, S.J. 1991. Gibberellin perception at the plasma membrane of Avena fatua aleurone protoplasts. Planta 183: 274-280.

    Article  Google Scholar 

  • Hotze, M., Waitz, A. and Schroder, J. 1994. cDNA for a 14-kilodalton polypeptide from Madagascar periwinkle (Catharanthus roseus). Plant Physiol. 104: 1097-1098.

    PubMed  Google Scholar 

  • Huang, Y.-F., Jordan, W.R., Wing, R.A. and Morgan, P.W. 1998. Gene expression induced by physical impedance in maize roots. Plant Mol. Biol. 37: 921-930.

    PubMed  Google Scholar 

  • Ito, T., Kito, K., Adati, N., Mitsui, Y., Hagiwara, H. and Sasaki, Y. 1994. Fluorescent differential display: arbitrarily primed RTPCR fingerprinting on an automated DNA sequencer. FEBS Lett. 351: 231-236.

    PubMed  Google Scholar 

  • Jackson, D.P. 1991. In situ hybridization in plants. In: D.J. Bowles, S.J. Gurr and M. McPhereson (Eds.), Molecular Plant Pathology: A practical Approach. Oxford University Press, Oxford, pp. 163-174.

    Google Scholar 

  • Jacobsen, J.V. and Beach, L.R. 1985. Control of transcription of _-amylse and rRNA genes in barley aleurone protoplasts by gibberellin and abscisic acid. Nature 316: 275-277.

    Google Scholar 

  • Jacobsen, S.E., Binkowski, K.A. and Olszewski, N.E. 1996. SPINDLY, a tetratricopeptide repeat protein involved in gibberellin signal transduction in Arabidopsis. Proc. Natl. Acad. Sci. USA 93: 9292-9296.

    PubMed  Google Scholar 

  • Jacobsen, S.E. and Olszewski, N.E. 1993. Mutations at the SPINDLY locus of Arabidopsis alter gibberellin signal transduction. Plant Cell 5: 887-896.

    Article  PubMed  Google Scholar 

  • Jones, H.D., Smith, S.J., Desikan, R., Plakidou-Dymock, S. and Lovegrove, A. 1998. Heterotrimeric G proteins are implicated in gibberellin induction of _-amylase gene expression in wild oat aleurone. Plant Cell 10: 245-253.

    PubMed  Google Scholar 

  • Kazama, H. and Katsumi, M. 1986. Biphasic response of cucumber hypocotyl sections to auxin. Plant Cell Physiol. 17: 467-473.

    Google Scholar 

  • Koornneef, M. and van der Veen, J.H. 1980. Induction and analysis of gibberellin sensitive mutants in Arabidopsis thaliana (L.) Heynh. Theor. Appl. Genet. 58: 257-263.

    Google Scholar 

  • Koornneef, M., Elgersma, A., Hanhart, C.J., van Loenen-Martinet, E.P., van Rijn, L. and Zeevaart, J.A.D. 1985. A gibberellin insensitive mutant of Arabidopsis thaliana. Physiol. Plant. 65: 33-39.

    Google Scholar 

  • Kuo, A., Cappelluti, S., Cervantes-Cervantes, M., Rodriguez, M. and Bush, D.S. 1996. Okadaic acid, a protein phosphatase inhibitor, blocks calcium changes, gene expression, and cell death induced by gibberellin in wheat aleurone cells. Plant Cell 8: 259-269.

    PubMed  Google Scholar 

  • Kutschera, U., Bergfed, R., Schopher, P. 1987. Cooperation of epidermis and inner tissues in auxin-mediated growth of maize coleoptiles. Planta 170: 168-180.

    Google Scholar 

  • Matsuo, T., Futsuhara, Y., Fumio, K. and Yamaguchi, H. 1997. In: Science of the Rice Plant, Rural Culture Association, pp. 300-317.

  • Murakami, Y. 1970. Dwarfing genes in rice and their relation to gibberellin biosynthesis. In: D.J. Carr (Ed.), Plant Growth Substances. Springer-Verlag, Berlin, pp. 166-174.

    Google Scholar 

  • Nakai, K. and Kanehisa, M. 1992. A knowledge base for predicting protein localization sites in eukaryotic cells. Genomics 14: 897-911.

    Google Scholar 

  • Peng, J., Carol, P., Richards, D.E., King, K.E., Cowling, R.J., Murphy G.P. and Harberd, N.P. 1997. The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Genes Dev. 11: 3194-3205.

    PubMed  Google Scholar 

  • Penson, S.P., Schuurink, R.C., Fath, A., Gubler, F., Jacobsen, J.V. and Jones, R.L. 1996. cGMP is required for gibberellic acid-induced gene expression in barley aleurone. Plant Cell 8: 2325-2333.

    PubMed  Google Scholar 

  • Phillips, A.L. and Huttly, A.K. 1994. Cloning of two gibberellinregulated cDNAs from Arabidopsis thaliana by subtractive hybridization: expression of the tonoplast water channel,-TIP, is increased by GA3. Plant Mol. Biol. 24: 603-615.

    PubMed  Google Scholar 

  • Phinney, B.O. 1996. Growth response of single-gene dwarf mutants in maize to gibberellic acid. Proc. Natl. Acad. Sci. USA 42: 185-189.

    Google Scholar 

  • Rasmusson, J. 1927. Genetically changed linkage values in Pisum. Hereditas 10: 1-150.

    Google Scholar 

  • Richards, K.D. and Gardner, R.C. 1995. pEARLI1 (accession No. L43080): an Arabidopsis member of a conserved gene family. Plant Physiol. 109: 1497.

  • Sakai, S. and Katsumi, M. 1994. Properties of gibberellin-binding proteins from normal and Dwarf-8 (a dominant gibberellin nonresponding dwarf mutant) seedlings of Zea mays L. Biosci. Biotechnol. Biochem. 58: 1340-1342.

    Google Scholar 

  • Shi, L., Gast, R.T., Gopalraj, M. and Olszewski, N.E. 1992. Characterization of a shoot-specific, GA3-and ABA-regulated gene from tomato. Plant J. 2: 153-159.

    Article  PubMed  Google Scholar 

  • Showalter, A.M. 1993. Structure and function of plant cell wall proteins. Plant Cell 5: 9-23.

    Article  PubMed  Google Scholar 

  • Silverstone, A.L., Ciampaglio, C.N. and Sun, T.-p. 1998. The arabidopsis RGA gene encodes a transcriptional regulator repressing the gibberellin signal transduction pathway. Plant Cell 10: 155-169.

    Article  PubMed  Google Scholar 

  • Speulman, E. and Salamini, F. 1995. GA3-regulated cDNAs from Hordeum vulgare leaves. Plant Mol. Biol. 28: 915-926.

    PubMed  Google Scholar 

  • Vinson, C.R., Sigler, P.B. and McKnight, S.L. 1989. Scissorsgrip model for DNA recognition by a family of leucine zipper proteins. Science 246: 911-916.

    PubMed  Google Scholar 

  • Walter, P., Gilmore, R. and Blobel, G. 1984. Protein translocation across the endoplasmic reticulum. Cell 38: 5-8.

    PubMed  Google Scholar 

  • Winkler, R.G. and Freeling, M. 1994. Physiological genetics of the dominant gibberellin-nonresponsive maize dwarfs, Dwarf8 and Dwarf9. Planta 193: 341-348.

    Google Scholar 

  • Xu, Y., Buchholz, W.G., DeRose, R.T. and Hall, T.C. 1995. Characterization of a rice gene family encoding root-specific proteins. Plant Mol. Biol. 27: 237-248.

    PubMed  Google Scholar 

  • Ye, Z.-H., Song, Y.-R., Marcus, A. and Varner, J.E., 1991. Comparative localization of three classes of cell wall proteins. Plant J. 1: 175-183.

    PubMed  Google Scholar 

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Authors and Affiliations

  1. Research and Education Center for Genetic Information, Nara Institute of Science and Technology, Ikoma, Nara, 630-0101, Japan

    M. Ogawa, T. Kusano, N. Koizumi & H. Sano

  2. Biology Department, International Christian University, Mitaka, Tokyo, 181-0015, Japan

    M. Katsumi

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  1. M. Ogawa
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  2. T. Kusano
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  3. N. Koizumi
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  4. M. Katsumi
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  5. H. Sano
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Ogawa, M., Kusano, T., Koizumi, N. et al. Gibberellin-responsive genes: high level of transcript accumulation in leaf sheath meristematic tissue from Zea mays L.. Plant Mol Biol 40, 645–657 (1999). https://doi.org/10.1023/A:1006291917591

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