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A role for gibberellic acid in orienting microtubules and regulating cell growth polarity in the maize root cortex

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Abstract

The role of gibberellins and cortical microtubules in determining the polarity of cell growth in the root cortex of maize (Zea mays L.) was examined. Inhibition of gibberellin biosynthesis, either naturally through mutation (d5 mutant) or by means of chemicals such as 2S,3S paclobutrazol, caused thickening of root apices and increased their starch content. Immunofluorescence microscopy of cortical microtubules, coupled with a comparison of cell widhts, lengths and shapes, indicated that the meristem and immediate post-mitotic zone were the targets of gibberellin deficiency. Cortical cells in these regions were impaired in their ability to develop highly ordered transversal arrays of cortical microtubules. Consequently, the cells became wider and shorter. Application of gibberellic acid re-established the arrangements of cortical microtubules and the polarity of cell growth characteristic for roots having normal levels of gibberellins, it also decreased the starch content. These results indicate that gibberellins are morphogenetically active substances, not only in shoots but also in roots of maize.

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Abbreviations

CMT:

cortical microtubule

GA:

gibberellin

GA3 :

gibberellic acid

MT:

microtubule

PIG:

postmitotic isodiametric growth

References

  • Akashi, T., Shibaoka, H. (1987) Effects of gibberellin on the arrangement and the cold stability of cortical microtubules in epidermal cells of pea internodes. Plant Cell Physiol. 28, 339–348

    Google Scholar 

  • Baluška, F., Kubica, Š., Hauskrecht, M. (1990) Postmitotic ‘isodiametric’ cell growth in the maize root apex. Planta 181, 269–274

    Google Scholar 

  • Baluška, F., Parker, J.S., Barlow, P.W. (1992) Specific patterns of cortical and endoplasmic microtubules associated with cell growth and tissue differentiation in roots of maize (Zea mays L.). J. Cell Sci. 103, 191–200

    Google Scholar 

  • Baluška, F., Parker, J.S., Barlow, P.W. (1993) The microtubular cytoskeleton in cells of cold-treated roots of maize (Zea mays L.) shows tissue-specific responses. Protoplasma 172, 84–96

    Google Scholar 

  • Barlow, P.W. (1992) The meristem and quiescent centre in cultured root apices of the gib-1 mutant of tomato Lycopersicon esculentum Mill. Ann. Bot. 69, 533–543

    Google Scholar 

  • Barlow, P.W., Brain, P., Parker, J.S. (1991) Cellular growth in roots of a gibberellin-deficient mutant of tomato (Lycopersicon esculentum Mill.) and its wild-type. J. Exp. Bot. 42, 339–351

    Google Scholar 

  • Bergfeld, R., Speth, V. Schopfer, P. (1988) Reorientation of microfibrils and microtubules at the outer epidermal wall of maize coleoptiles during auxin-mediated growth. Bot. Acta 101, 57–67

    Google Scholar 

  • Browning, G., Saunders, P.F. (1977) Membrane localized gibberellins A9 and A4 in wheat chloroplasts. Nature 265, 375–377

    Google Scholar 

  • Butcher, D.N., Appleford, N.E.J., Hedden, P., Lenton, J.R. (1988) Plant growth substances in root cultures of Lycopersicon esculentum. Phytochemistry 27, 1575–1578

    Google Scholar 

  • Butcher, D.N., Clark, J.A., Lenton, J.R. (1990) Gibberellins and the growth of excised tomato roots: Comparison of gib-1 mutant and wild type and responses to applied GA3 and 2S,3S paclobutrazol. J. Exp. Bot. 41, 715–722

    Google Scholar 

  • Cosgrove, D.J., Sovonick-Dunford, S.A. (1989) Mechanism of gibberellin-dependent stem elongation in peas. Plant Physiol. 89, 184–191

    Google Scholar 

  • Davidonis, G.H. (1990) Gibberellic acid-induced cell elongation in cotton suspension cultures. J. Plant Growth Regul. 9, 243–246

    Google Scholar 

  • Ishida, K., Katsumi, M. (1991) Immunofluorescence microscopical observation on cortical microtubule arrangement as affected by gibberellin in d5 mutant of Zea mays L. Plant Cell Physiol. 32, 409–417

    Google Scholar 

  • Ishikawa, H., Evans, M.L. (1992) Induction of curvature in maize roots by calcium or by thigmostimulation. Role of the postmitotic isodiametric growth zone. Plant Physiol. 100, 762–768

    Google Scholar 

  • Jupe, S.C., Causton, D.R., Scott, I.M. (1988) Cellular basis of the effects of gibberellin and the pro gene on stem growth in tomato. Planta 174, 106–111

    Google Scholar 

  • Katsumi, M., Ishida, K. (1989) The gibberellin control of cell elongation. In: Gibberellins, pp. 211–219, Takahashi, N., Phinney, B.O., MacMillan, J., eds. Springer Verlag, New York

    Google Scholar 

  • Keyes, G., Sorrells, M.E., Setter, T.L. (1990) Gibberellic acid regulates cell wall extensibility in wheat (Triticum aestivum L.) Plant Physiol. 92, 242–245

    Google Scholar 

  • Kubica, S., Baluška, F., Hauskrecht, M. (1991) Elemental growth rate and rRNA transcript maturation exhibit the same pattern in individual tissues of the maize root apex. Ann. Bot. 68, 387–391

    Google Scholar 

  • Lloyd, C.W., Slabas, A.R., Powell, A.J., Lowe, S.B. (1980) Microtubules, protoplasts and plant cell shape: An immunofluorescent study. Planta 147, 500–506

    Google Scholar 

  • Marc, J., Hackett, W.P. (1989) A new method for immunofluorescent localization of microtubules in surface cell layers: application to the shoot apical meristem of Hedera. Protoplasma 148, 70–79

    Google Scholar 

  • Marc, J., Hackett, W.P. (1992) Changes in the pattern of cell arrangement at the surface of the shoot apical meristem in Hedera helix L. following gibberellin treatment. Planta 186, 503–510

    Google Scholar 

  • Mita, T., Katsumi, M. (1986) Gibberellin control of microtubule arrangement in the mesocotyl epidermal cells of the d5 mutant of Zea mays L. Plant Cell Physiol. 27, 651–659

    Google Scholar 

  • Mita, T., Shibaoka, H. (1984) Gibberellin stabilizes microtubules in onion leaf sheath cells. Protoplasma 119, 100–109

    Google Scholar 

  • Nakagawa, S., Tjokrokusumo, D.S., Sakurai, A., Yamaguchi, I., Takahashi, N., Syono, K. (1987) Endogenous levels of gibberellins, IAA and cytokinins in tobacco crown gall tissues of different morphologies. Plant Cell Physiol. 28, 485–493

    Google Scholar 

  • Park, K.-H., Fujisawa, S., Sakurai, A., Yamaguchi, I., Takahashi, N. (1984) Changes in endogenous gibberellin contents during growth of cultured tobacco cells. Plant Cell Physiol. 25, 1303–1306

    Google Scholar 

  • Phinney, B.O. (1985) Gibberellin A1 dwarfism and shoot elongation in higher plants. Biol. Plant. 27, 172–179

    Google Scholar 

  • Robertson, E.J. (1991) A cytological study of the musci. Ph. D. thesis, University of London, UK

    Google Scholar 

  • Seagull, R.W. (1986) Changes in microtubule organization and microfibril orientation during in vitro cotton fiber development. Can. J. Bot. 64, 1373–1381

    Google Scholar 

  • Seagull, R.W. (1992) A quantitative electron microscopic study of changes in microtubule arrays and wall microfibril orientation during in vitro cotton fiber development. J. Cell Sci. 101, 561–577

    Google Scholar 

  • Shibaoka, H. (1974) Involvement of wall microtubules in gibberellin promotion and kinetin inhibition of stem elongation. Plant Cell Physiol. 15, 155–163

    Google Scholar 

  • Simcox, P.D., Dennis, D.T., West, C.A. (1975) Kaurene synthetase from plastids of developing plant tissues. Biochem. Biophys. Res. Commun. 66, 166–172

    Google Scholar 

  • Simmonds, D., Setterfield, G., Brown, D.L. (1983) Organization of microtubules in dividing and elongating cells of Vicia hajastana Grossh. in suspension culture. Eur. J. Cell. Biol. 32, 59–66

    Google Scholar 

  • Tanimoto, E. (1987) Gibberellin-dependent root elongation in Lactuca sativa: Recovery from growth retardant-suppressed elongation with thickening by low concentration of GA3. Plant Cell Physiol. 28, 963–973

    Google Scholar 

  • Tanimoto, E. (1988) Gibberellin regulation of root growth with change in galactose content of cell walls in Pisum sativum. Plant Cell Physiol. 29, 269–280

    Google Scholar 

  • Tanimoto, E. (1991) Gibberellin requirement for the normal growth of roots. In: Gibberellins, pp. 229–240, Takahashi, N., Phinney, B.O., MacMillan, J., eds. Springer Verlag, New York

    Google Scholar 

  • Taylor, A., Cosgrove, D.J. (1989) Gibberellic acid stimulation of cucumber hypocotyl elongation. Effects on growth, turgor, osmotic pressure, and cell wall properties. Plant Physiol. 90, 1335–1340

    Google Scholar 

  • Upadhyaya, M.K., Nooden, L.D. (1978) Relationship between the induction of swelling and the inhibition of elongation caused by oryzalin and colchicine in corn roots. Plant Cell Physiol. 19, 133–138

    Google Scholar 

  • Weerdenburg, C., Seagull, R.W. (1988) The effects of taxol and colchicine on microtubule and microfibril arrays in elongating plant cells in culture. Can. J. Bot. 66, 1707–1716

    Google Scholar 

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The authors acknowledge the support to F.B. from the Royal Society (London UK). We also thank Dr. J. Lenton (University of Bristol, Long Ashton Research Station) who kindly supplied us with 2S,3S paclobutrazol and grains of the GA-deficient d5 mutant of maize.

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Baluška, F., Parker, J.S. & Barlow, P.W. A role for gibberellic acid in orienting microtubules and regulating cell growth polarity in the maize root cortex. Planta 191, 149–157 (1993). https://doi.org/10.1007/BF00199744

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  • DOI: https://doi.org/10.1007/BF00199744

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