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Mechano-sensitive orientation of cortical microtubules during gravitropism in azuki bean epicotyls

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Abstract

The orientation of cortical microtubules (cMT) during gravitropism was studied in epidermal cells of azuki epicotyls. The relative proportion of cells with longitudinal cMT increased in the upper epidermis, and those with transverse cMT increased in the lower epidermis. When epicotyls were kept straight during gravistimulation, no change in cMT orientation occurred in either the upper and lower epidermis. When epicotyls were forced to bend downward, cells with transverse cMT increased in the upper epidermis, and those with longitudinal cMT increased in the lower epidermis. When epicotyls were loaded with naphthylphthalamic acid, an inhibitor of auxin transport, both gravitropic bending and change in cMT orientation were inhibited. However, when a change in cMT orientation was induced by forced downward bending, cells with longitudinal cMT increased in the compressed (lower) side and those with transverse cMT increased in the extended (upper) side. It was suggested that cMT orientation was controlled by the bending of the epicotyl and not by a gravity signal per se. Loading with Gd3+, an inhibitor of the stretch-activated channel, did not inhibit gravitropic bending. However, it inhibited cMT reorientation induced by gravitropic bending and by forced bending. Involvement of the stretch-activated channel in mechano-sensitive orientation of cMT was suggested.

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References

  • Baluska F, Hauskrecht M, Barlow PW, Sievers A (1996) Gravitropism of the primary root of maize: a complex pattern of differential cellular growth in the cortex independent of the microtubular cytoskeleton. Planta 198:310–318

    Google Scholar 

  • Blancaflor EB, Hasenstein KH (1993) Organization of cortical microtubules in graviresponding maize roots. Planta 191:231–237

    Google Scholar 

  • Cosgrove DJ, Hedrich R (1991) Stretch-activated chloride, potassium, and calcium channels coexisting in plasma membranes of guard cells of Vicia faba L. Planta 186:143–153

    Article  Google Scholar 

  • Cyr RJ, Palevitz BA (1995) Organization of cortical microtubules in plant cells. Curr Opin Cell Biol 7:65–71

    Article  CAS  PubMed  Google Scholar 

  • Delmer DP (1999) Cellulose biosynthesis: exciting times for a difficult field of study. Annu Rev Plant Physiol Plant Mol Biol 50:245–276

    Article  CAS  PubMed  Google Scholar 

  • Ding JP, Pickard BG (1993) Mechanosensory calcium-selective cation channels in epidermal cells. Plant J 3:83–110

    Article  Google Scholar 

  • Emons AMC, Mulder BM (2000) How the deposition of cellulose microfibrils builds cell architecture. Trends Plant Sci 5:35–40

    Article  Google Scholar 

  • Falke LC, Edwards KL, Pickard BG, Misler S (1988) A stretch-activated anion channel in tobacco protoplasts. FEBS Lett 237:141–144

    Article  Google Scholar 

  • Fischer K, Schopfer P (1997) Interaction of auxin, light, and mechanical stress in orienting microtubules in relation to tropic curvature in the epidermis of maize coleoptiles. Protoplasma 196:108–116

    Google Scholar 

  • Fischer K, Schopfer P (1998) Physical strain-mediated microtubule reorientation in the epidermis of gravitropically stimulated maize coleoptiles. Plant J 15:119–123

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Hasenstein KH, Blancaflor EB, Lee JS (1999) The microtubule cytoskeleton does not integrate auxin transport and gravitropism in maize roots. Physiol Plant 105:729–38

    Article  Google Scholar 

  • Himmelspach R, Wymer CL, Lloyd CW, Nick P (1999) Gravity-induced reorientation of cortical microtubules observed in vivo. Plant J 18:449–453

    Article  Google Scholar 

  • Inoue N, Yamada S, Nagata Y, Shimmen T (2002) Rhizoid differentiation in Spirogyra: position sensing by terminal cells. Plant Cell Physiol 43:479–483

    CAS  PubMed  Google Scholar 

  • Iwata K, Hogetu T (1989) The effects of light irradiation on the orientation of microtubules in seeding of Avena sativa L. and Pisum sativaum L. Plant Cell Physiol 30:1011–1016

    Google Scholar 

  • Iwata K, Tazawa M, Itoh T (2001) Turgor pressure regulation and orientation of cortical microtubules in Spirogyra cells. Plant Cell Physiol 42:594–598

    Article  Google Scholar 

  • Kaneko T, Saito C, Shimmen T, Kikuyama M (2005) Possible involvement of mechanosensitive Ca2+ channels of plasma membrane in mechanoperception in Chara. Plant Cell Physiol 46 (in press)

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    PubMed  Google Scholar 

  • Lambert AM (1993) Microtubule-organizing centers in higher plants. Curr Opin Cell Biol 5:116–122

    Google Scholar 

  • Lloyd CW (1987) The plant cytoskeleton: the impact of fluorescence microscopy. Annu Rev Plant Physiol 38:119–139

    Article  Google Scholar 

  • Mayumi K, Shibaoka H (1995) A possible double role for brassinolide in the reorientation of cortical microtubules in the epidermal cells of azuki bean epicotyls. Plant Cell Physiol 36:173–181

    CAS  Google Scholar 

  • Mayumi K, Shibaoka H (1996) The cyclic reorientation of cortical microtubules on walls with a crossed polylamellate structure: effect of plant hormones and an inhibitor of protein kinases on progression of the cycle. Protoplasma 195:112–122

    CAS  Google Scholar 

  • Mizuno K (1994) Inhibition of gibberellin-induced elongation, reorientation of cortical microtubules and change of isoform of tubulin in epicotyl segments of azuki bean by protein kinase inhibitors. Plant Cell Physiol 35:1149–1157

    Google Scholar 

  • Nick P, Bergfeld R, Schafer E, Schopfer P (1990) Unilateral reorientation of microtubules at the outer epidermal wall during photo- and gravi-tropic curvature of maize coleoptiles and sunflower hypocotyls. Planta 181:162–168

    Article  Google Scholar 

  • Nick P, Schopfer E, Hertel R, Furuya M (1991) On the putative role of microtubules in gravitropism of maize coleoptiles. Plant Cell Physiol 32:873–880

    Google Scholar 

  • Pickard BG, Ding JP (1993) The mechanosensory calcium-selective ion channel: key component of a plasmalemmal control centre? Aust J Plant Physiol 20:439–459

    Google Scholar 

  • Roberts KR, Farmer MA, Schneider RM, Lemoine JE (1988) The microtubular cytoskeleton of Amphidinium rhychocephalum (Dinophycease). J Phycol 24:544–553

    Google Scholar 

  • Sato Y, Wada M, Kadota A (2001) External Ca2+ is essential for chloroplast movement induced by mechanical stimulation but not by light stimulation. Plant Physiol 127:497–504

    Article  Google Scholar 

  • Sawano M, Sonobe S, Shimmen T (2000) Possible involvement of 65 kDa MAP in epicotyl in azuki bean. Plant Cell Physiol 41:968–976

    Article  Google Scholar 

  • Shibaoka H (1991) Microtubule and the regulation of cell morphogenesis by plant hormone. In: Lloyd CW (ed) The cytoskeletal basis of plant growth and form. Academic Press, London, pp 159–168

    Google Scholar 

  • Shibaoka H (1994) Plant hormone-induced changes in the orientation of cortical microtubules: alterations in the cross-linking between microtubules and the plasma membrane. Annu Rev Plant Physiol Plant Mol Biol 45:527–544

    Google Scholar 

  • Shimmen T (1997) Studies on mechano-perception in Characeae: effect of external Ca2+ and Cl−. Plant Cell Physiol 38:691–697

    Google Scholar 

  • Takesue K, Shibaoka H (1998) The cyclic reorientation of cortical microtubules in epidermal cells of azuki bean epicotyl: the role of actin filaments in the progression of the cycle. Planta 205:539–546

    Article  Google Scholar 

  • Williamson RE (1990) Alignment of cortical microtubules by anisotropic wall stresses. Aust J Plant Physiol 17:601–613

    Google Scholar 

  • 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

    Google Scholar 

  • Zandomeni K, Schopfer P (1994) Mechanosensory microtubule reorientation in the epidermis of maize coleoptiles subjected to bending stress. Protoplasma 182(3–4):96–101

    Google Scholar 

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Authors and Affiliations

  1. Department of Life Science, Graduate School of Life Science, University of Hyogo, Harima Science Park City, Hyogo, 678-1297, Japan

    Toshimitsu Ikushima & Teruo Shimmen

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  1. Toshimitsu Ikushima
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  2. Teruo Shimmen
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Correspondence to Toshimitsu Ikushima.

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Ikushima, T., Shimmen, T. Mechano-sensitive orientation of cortical microtubules during gravitropism in azuki bean epicotyls. J Plant Res 118, 19–26 (2005). https://doi.org/10.1007/s10265-004-0189-8

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  • DOI: https://doi.org/10.1007/s10265-004-0189-8

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