Summary
Plants respond to mechanical stress by adaptive changes in growth. Although this phenomenon is well established, the mechanism of the perception of mechanical forces by plant cells is not yet known. We provide evidence that the cortical microtubules sub-adjacent to the growth-controlling outer epidermal cell wall of maize coleoptiles respond to mechanical extension and compression by rapidly reorientating perpendicular to the direction of the effective force change. These findings shed new light on many seemingly unrelated observations on microtubule reorientation by growth factors such as light or phytohormones. Moreover, our results suggest that microtubules associated with the plasma membrane are causally involved in sensing vectorial forces and provide vectorial information to the cell that can be utilized in the orientation of plant organ expansion.
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Abbreviations
- MT:
-
cortical microtubule
References
Baluska F, Parker JS, Barlow PW (1993) A role for gibberellic acid in orientating microtubules and regulating cell growth polarity in the maize root cortex. Planta 191: 149–157
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
Cleary AF, Hardham AR (1993) Pressure induced reorientation of cortical microtubules in epidermal cells ofLolium rigidum leaves. Plant Cell Physiol 34: 1003–1008
Doonan JH (1991) The cytoskeleton and moss morphogenesis. In: Lloyd CW (ed) The cytoskeletal basis of plant growth and form. Academic Press, London, pp 289–301
Edelmann H, Bergfeld R, Schopfer P (1989) Role of cell-wall biogenesis in the initiation of auxin-mediated growth in coleoptiles ofZea mays L. Planta 179: 486–494
Giddings TH, Staehelin LA (1991) Microtubule-mediated control of microfibril deposition: a re-examination of the hypothesis. In: Lloyd CW (ed) The cytoskeletal basis of plant growth and form. Academic Press, London, pp 85–99
Green PB (1963) On mechanisms of elongation. In: Locke M (ed) Cytodifferentiation and macromolecular synthesis. Academic Press, New York, pp 203–234
—, Selker ML (1991) Mutual alignments of cell walls, cellulose, and cytoskeletons: their role in meristems. In: Lloyd CW (ed) The cytoskeletal basis of plant growth and form. Academic Press, London, pp 302–322
Hohl M, Schopfer P (1992) Cell-wall tension of the inner tissue of the maize coleoptile and its potential contribution to auxin-mediated organ growth. Planta 188: 340–344
Hush JM, Overall RL (1991) Electrical and mechanical fields orient cortical microtubules in higher plant tissues. Cell Biol Int Rep 15: 551–560
—, Hawes CR, Overall RL (1990) Interphase microtubule re-orientation predicts a new cell polarity in wounded pea roots. J Cell Sci 96: 47–61
Iwata K, Hogetsu T (1989) The effects of light irradiation on the orientation of microtubules in seedlings ofAvena sativa L. andPisum sativum L. Plant Cell Physiol 30: 1011–1016
Kwon YH, Hoch HC, Aist JR (1991) Initiation of appressorium formation inUromyces appendiculatus: organization of the apex, and the responses involving microtubules and apical vesicles. Can J Bot 69: 2560–2573
Lintilhac PM, Vesecky TB (1981) Mechanical stress and cell wall orientation in plants. II. The application of controlled directional stress to growing plants; with a discussion on the nature of the wound reaction. Amer J Bot 68: 1222–1230
— — (1984) Stress-induced alignment of division plane in plant tissues grown in vitro. Nature 307: 363–364
Mita T, Shibaoka H (1984) Effect of S-3307, an inhibitor of gibberellin biosynthesis, on swelling of leaf sheath cells and on the arrangement of cortical microtubules in onion seedlings. Plant Cell Physiol 25: 1531–1539
Nick P, Bergfeld R, Schäfer E, Schopfer P (1990) Unilateral reorientation of microtubules at the outer epidermal wall during photo- and gravitropic curvature of maize coleoptiles and sunflower hypocotyls. Planta 181: 162–168
Rasdorsky W (1925) Über die Reaktion der Pflanzen auf die mechanische Inanspruchnahme. Ber Dtsch Bot Ges 43: 332–352
Selker JML (1990) Microtubule patterning in apical epidermal cells ofVinca minor preceding leaf emergence. Protoplasma 158: 95–108
Shibaoka H (1991) Microtubules and the regulation of cell morphogenensis by plant hormones. In: Lloyd CW (ed) The cytoskeletal basis of plant growth and form. Academic Press, London, pp 159–168
Wada M, Murata T (1991) The cytoskeleton in fern protonemal growth in relation to photomorphogenesis. In: Lloyd CW (ed) The cytoskeletal basis of plant growth and form. Academic Press, London, pp 277–288
Wang N, Butler JP, Ingber DE (1993) Mechanotransduction across the cell surface and through the cytoskeleton. Science 260: 1124–1127
White RG, Hyde GJ, Overall RL (1990) Microtubule arrays in regeneratingMougeotia protoplasts may be oriented by electrical fields. Protoplasma 158: 73–85
Williamson RE (1990) Alignment of cortical microtubules by anisotropic wall stresses. Aust J Plant Physiol 17: 601–613
— (1991) Orientation of cortical microtubules in interphase plant cells. Int Rev Cytol 129: 135–206
Wilson BF, Archer RR (1977) Reaction wood: induction and mechanical action. Annu Rev Plant Physiol 28: 23–43
Zandomeni K, Schopfer P (1993) Reorientation of microtubules at the outer epidermal wall of maize coleoptiles by phytochrome, blue-light photoreceptor, and auxin. Protoplasma 173: 103–112
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Zandomeni, K., Schopfer, P. Mechanosensory microtubule reorientation in the epidermis of maize coleoptiles subjected to bending stress. Protoplasma 182, 96–101 (1994). https://doi.org/10.1007/BF01403471
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DOI: https://doi.org/10.1007/BF01403471