Cortical microtubule reorientation in higher plants: Dynamics and regulation

Journal of Microscopy

Volumn 181, Issue 2, 1996, Pages 129-139

  Hush, J M ^a   Overall, R L ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Cortical microtubules; Electric field; Extracellular matrix; Mechanical forces; Microtubule dynamics; Orientation mechanisms; Plant cell; Wounding

Indexed keywords

CELLS; ENVIRONMENTAL REGULATIONS; PLANT CELL CULTURE;

CORTICAL MICROTUBULE; EXTRACELLULAR MATRICES; HIGHER PLANTS; LIVE CELL; MECHANICAL FORCE; MICROTUBULE DYNAMICS; MICROTUBULES; ORIENTATION MECHANISM; PLANTS CELLS; WOUNDING;

ELECTRIC FIELDS;

ARTICLE; DYNAMICS; ELECTRIC FIELD; MICROSCOPY; MICROTUBULE; PLANT CELL; PRIORITY JOURNAL;

EMBRYOPHYTA;

EID: 0029988463     PISSN: 00222720     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2818.1996.106386.x     Document Type: Article

References (91)

1. Asada, T. & Shibaoka, H. (1994) Isolation of polypetides with microtubule-translocating activity from phragmoplasts of tobacco BY-2 cells. J. Cell Sci. 107, 2249-2257.
2. 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.
3. Baskin, T.I. & Williamson, R.E. (1992) Ethylene, microtubules and root morphology in wild-type and mutant Arabidopsis seedlings. Current Top. Plant Biochem. Physiol. 11, 118-130.
4. 2+-binding proteins. Proc. Natl. Acad. Sci. 83, 5512-5516.
5. 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.
6. Blackman, L.M. & Overall, R.L. (1995) Electric fields affect the orientation of cortical microtubules and cell expansion in pea callus. Protoplasma, in press.
7. Blancaflor, E.B. & Hasenstein, K.H. (1995) Time course and auxin sensitivity of cortical microtubule reorientation in maize roots. Protoplasma, 185, 72-82.
8. Braam, J. (1992) Regulation of expression of calmodulin and calmodulin-related genes by environmental stimuli in plants. Cell Calcium, 13, 457-463.
9. Bryant, G. & Wolf, J. (1987) Electromechanical stresses produced in the plasma membranes of suspended cells by applied electric fields. J. Memb. Biol. 96, 129-139.
10. Buxbaum, R.E. & Heidemann, S.R. (1988) A thermodynamic model for force integration and microtubule assembly during axonemal elongation. J. Theor. Biol. 134, 379-390.
11. Cheung, W.Y. (1980) Calcium and Cell Function, Vol. 1. Calmodulin. Academic Press.
12. Chu, B., Snustad, D.P. & Carter, J.B. (1993) Alteration of β-tubulin gene expression during low-temperature exposure in leaves of Arabidopsis thaliana. Plant Physiol. 103, 371-377.
13. Cleary, A.L., Gunning, B.E.S., Wasteneys, G.O. & Hepler, P.K. (1992) Microtubule and F-actin dynamics at the division site in living Tradescantia stamen hair cells. J. Cell Sci. 103, 977-988.
14. Cleary, A.L. & Hardham, A.R. (1993) Pressure induced reorientation of cortical microtubules in epidermal cells of Lolium rigidum leaves. Plant Cell Physiol. 34, 1003-1008.
15. Cohen, P. & Klee, C.B. (eds) (1988) Calmodulin, Molecular Aspects of Cellular Regulation. Elsevier, New York.
16. Cyr, R.J. (1991) Calcium/calmodulin affects microtubule stability in lysed protoplasts. J. Cell Sci. 100, 311-317.
17. Cyr, R.J. (1994) Microtubules in plant morphogenesis: role of the cortical array. Ann. Rev. Cell Biol. 10, 153-180.
18. Cyr, R.J. & Palevitz, B.A. (1989) Microtubule-binding proteins from carrot. Planta, 177, 245-260.
19. Cyr, R.J. & Palevitz, B.A. (1995) Organization of cortical microtubules in plant cells. Curr. Op. Cell Biol. 7, 65-71.
20. Ding, J.P. & Pickard, B.G. (1993) Mechanosensory calcium-selective cation channels in epidermal cells. Plant J. 3, 83-110.
21. Gilroy, S., Blowers, D. P. & Trewavas, A.J. (1987) Calcium: a regulation system emerges in plant cells. Development, 100, 181-184.
22. Goddard, R.H., Wick, S.M., Silflow, C.D. & Snustad, D.P. (1994) Microtubule components of the plant cell cytoskeleton. Plant Physiol. 104, 1-6.
23. Hardham, A.R. (1982) Regulation of polarity in tissues and organs. In: The Cytoskeleton in Plant Growth and Development (ed. by C. W. Lloyd). pp. 577-405, Academic Press.
24. Hardham, A.R., Green, P.B. & Lang, J.M. (1980) Reoganization of cortical microlubules and cellulose deposition during leaf formation in Graptopetalum. Planta. 149, 181-195.
25. Hayashi, R., Morikawa, R., Nakajima, N., Ichikawa, Y. & Senda, M. (1980) Oriented structure of pectic polysaccharides in pea epidermal cell walls. Plant Cell Physiol. 21, 999-1005.
26. Hepler, P.K. & Wayne, R.O. (1985) Calcium and plant development. Ann. Rev. Plant Physiol. 25, 309-362.
27. Hogetsu, T. & Oshima, Y. (1986) Immunofluorescence microscopy of microtubule arrangement in root cells of Pisum sativum L. var Alaska. Plum Cell Physiol. 27, 939-945.
28. Holdaway, N.J., White, R.G. & Overall, R.L. (1995) Is the recovery of microtubule orientation in pea roots dependent on the cell wall? Cell Biol. Int. (in press).
29. Hush, J.M., Hawes, C.R. & Overall, R.L. (1990) Interphase microtubule re-orientation predicts a new cell polarity in wounded pea roots. J. Cell Sci. 96, 47-61.
30. Hush, J.M., Newman, I.A. & Overall, R.L. (1992) Utilization of the vibrating probe and ion-selective microelectrode techniques to investigate electrophysiological responses to wounding in pea roots. J. Exp. Bot. 43, 1251-1257.
31. Hush, J.M. & Overall, R.L. (1989) Steady ionic currents around pea (Pisum sativum L.) root tips: the effects of tissue wounding. Biol. Bull. 176, 56-64.
32. Hush, J.M. & Overall, R.L. (1991) Electrical and mechanical fields orient cortical microtubules in higher plant tissue. Cell Biol. Int. Rep. 15, 551-560.
33. Hush, J. M. & Overall, R.L. (1992) Re-orientation of cortical F-actin is not necessary for wound-induced microtubule re-orientation and cell polarity establishment. Protoplasma. 169, 97-106.
34. Hush, J.M., Overall, R.L. & Newman, I.A. (1991) A calcium influx precedes organogenesis in Graptopetalum. Plant. Cell Environ. 14, 657-665.
35. Hush, J.M., Wadsworth, P., Callaham, D.A. & Hepler, P.K. (1994) Quantification of microtubule dynamics in living plant cells using fluorescence redistribution after photobleaching. J. Cell Sci. 107, 775-784.
36. Hush, J.M., Wu, L., John, P.C.L., Hepler, L.H. & Hepler, P.K. (1996) Plant mitosis promoting factor disassembles the microtubule preprophase band and accelerates prophase progression in Tradescantia. Cell Biol. Int. (in press).
37. Hussey, P.J., Traas, J.A., Gull, K. & Lloyd, C.W. (1987) Isolation of cytoskeletons from synchronized plant cells: the interphase microtubule array utilizes multiple tubulin isotypes. J. Cell Sci. 88, 225-230.
38. Ingber, D.E., Dike, L., Hansen, L., Karp, S., Liley, H., Maniotis, A., McNamee, H., Mooney, D. Plopper, G., Sims, J. & Wang, N. (1994) Cellular tensegrity: exploring how mechanical changes in the cytoskeleton regulate cell growth, migration and tissue pattern during morphogenesis. Int. Rev. Cytol. 150, 173-224.
39. Ishida, K. & Katsumi, M. (1992) Effects of gibberellin and abscisic acid on the cortical microtubule orientation in hypocotyl cells of light-grown cucumber seedlings. Int. J. Plant Sci. 153, 155- 163.
40. Iwata, K. & Hogetsu, T. (1989) The effects of light irradiation on the orientation of microtubules in seedlings of Avena sativa. L. & Pisum sativum L. Plant Cell Physiol. 30, 1011-1016.
41. Jaffe, L.F. & Nuccitelli, R. (1977) Electrical controls of development. Ann. Rev. Biophys. Bioeng. 6, 445-476.
42. Knight, M.R., Campbell, A.K., Smith, S.M. & Trewavas, A.J. (1991) Transgenic plant aequorin reports the effects of touch and cold- shock and elicitors on cytoplasmic calcium. Nature, 352, 524-526.
43. Knight, M.R., Read, N.D., Campbell, A.K. & Trewavas, A.J. (1993) Imaging calcium dynamics in living plants using semi-synthetic recombinant Aequorins. J. Cell Biol. 121, 83-90.
44. Kobayashi, H., Fukuda, H. & Shibaoka, H. (1988) Interrelationship between the spatial deposition of actin filaments and microtubules during the differentiation of tracheary elements in cultured Zinnia cells. Protoplasma. 143, 29-37.
45. Kuss-Wymer, C. (1994) Microtubule cortical array reorientation and stability in plant cells. PhD thesis, Pennsylvania State University of College Park, PA.
46. Laskowski, M. (1990) Microtubule orientation in pea stem cells: a change in orientation follows the initiation of growth rate decline. Planta, 181, 44-52.
47. Lintilhac, P.M. (1974a) Differentiation, organogenesis and the tectonics of cell wall orientation. II. Separation of stresses in a two-dimensional model. Am. J. Bot. 61, 135-140.
48. Lintilhac, P.M. (1974b) Differentiation, organogenesis and the tectonics of cell wall orientation. III. Theoretical considerations of cell wall mechanics. Am. J. Bot. 61, 250-257.
49. Lipetz, J. (1970) Wound-healing in higher plants. Int. Rev. Cytol. 27, 1-28.
50. Liu, B., Marc, J., Joshi, H.C. & Palevitz, B.A. (1993) A γ-tubulin-related protein associates with the microtubule arrays of higher plants in a cell-cycle-dependent manner. J. Cell Sci. 104, 1217-1228.
51. Malhó, R., Read, N.D., Pais, M.S. & Trewavas, A.J. (1994) Role of cytosolic free calcium in the reorientation of pollen lube growth. Plant J. 5, 331-341.
52. Mayumi, K. & Shibaoka, H. (1995) A possible double role for brassinolide in the reorientation of cortical inicrotubules in the epidermal cells of azuki bean epicotyls. Plant Cell Physiol. 36, 173-181.
53. Meggs, W.J. (1988) Electric fields determine the spatial organization of microtubules and actin filaments. Med. Hypoth. 26, 165-170.
54. 3-induced elongation of oat internode segments. Plant Cell Physiol. 34, 975-985.
55. Mita, T. & Shibaoka, H. (1984) Giberrellin stabilizes microtubules in onion leaf sheath cells. Protoplasma, 119, 100-109.
56. Mitsui, H., Yamaguchi-Shinozaki, K., Shinozaki, K., Nishikawa, K. & Takahashi, H. (1995) Identification of a gene family (kat) encoding kinesin-like proteins in Arabidopsis thaliana and the characterization of secondary structure of katA. Mol. Gen. Genet. 238, 362-368.
57. 2+ messenger system in plants. Int. Rev. Cytol. 142, 305-345.
58. Nick, P., Bergfeld, R., Schäfer, E. & Schöpfer, 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.
59. Nuccitelli, R. (1990) Vibrating probe technique for studies of ion transport. In: Noninvasive Techniques in Cell Biology (ed. by J. K. Foskell and S. Grinstein), pp. 273-310. Wiley-Liss, New York.
60. Oakley, B.R., Oakley, C.E., Yoon, Y. & Jung, M.K. (1990) γ-tubulin is a component of the spindle pole body that is essential for microtubule function in Aspergillus nidulans. Cell. 61, 1289-1301.
61. Panda, D., Miller, H.P., Banerjee, A., Luduena, R.F. & Wilson, L. (1994) Microtubule dynamics in vitro are regulated by the tubulin isotype composition. Proc.Natl. Acad. Sci. 91, 11358-11362.
62. Roberts, I.N., Lloyd, C.W. & Roberts, K. (1985) Ethylene-induced microtubule reorientations: mediation by helical arrays. Planta, 164, 439-447.
63. Sachs, T. (1984) Axiality and polarity in vascular plants. In: Positional Controls in Plant Development (ed. by P. W. Barlow and D. J. Carr), pp. 193-224. Cambridge University Press.
64. Sakiyama, M. & Shibaoka, H. (1990) Effects of abscisic add on the orientation and cold stability of cortical microtubules in epicotyl cells of the dwarf pea. Protoplasma, 157, 165-171.
65. 3 and abscisic acid cause the reorientation of cortical microtubules in epicotyl cells of the decapitated dwarf pea. Plant Cell Physiol. 34, 431-437.
66. Sawhney, V.K. & Srivastava, L.M. (1974) Gibberellic acid-induced elongation of lettuce hypocolyls and its Inhibition by colchicine. Can. J. Bot. 52, 259-264.
67. Schellenbaum, P., Vantard, M., Fellous, A. & Lambert, A.-M. (1993) Co-assembly properties of higher plant microtubule-associated proteins with purified brain and plant tubulins. Plant J. 3, 253-260.
68. Schliwa, M., Euleneuer, U., Bulinski, J.C. & Izant, J.G. (1981) Calcium lability of cytoplasmic microtubules and its modification by microtubule associated proteins. Proc. Natl. Acad. Sci. 78, 413-418.
69. Seagull, R. W. (1990) The effects of microtubule and microfilament disrupting agents on cytoskeletal arrays and wall deposition in developing cotton fibres. Protoplasma, 159, 44-59.
70. Shibaoka, H. (1974) Involvement of wall microtubules in gibberellin promotion and kinelin inhibition of stem elongation. Plant Cell Physiol. 15, 255-263.
71. Shibaoka, H. (1993) Regulation by gibberellins of the orientation of cortical microtubules in plant cells. Aust. J. Plant Physiol. 20, 461-470.
72. Shibaoka, H. (1994) Plant hormone-Induced changes in the orientation of cortical microtubules: alterations in the cross- linking between microtubules and the plasma membrane. Ann. Rev. Plant Physiol. Plant Molec. Biol. 45, 527-544.
73. Steen, D.A. & Chadwick, A.V. (1981) Ethylene effects in pea stem tissue. Evidence for microtubule mediation. Plant Physiol. 67, 460-466.
74. Tiezzi, A., Moscatelli, A., Cai, G., Bartalesi, A. & Cresti, M. (1992) An immunoreactive homolog of mammalian kinesin in Nicotiana tabacum pollen tubes. Cell Motil. Cytoskel. 21, 132-137.
75. Traas, J.A., Doonan, J.H., Rawlins, D.J., Shaw, P.J., Watts, P.J. & Lloyd, C.W. (1987) An actin network is present in the cytoplasm throughout the cell cycle of carrot cells and associates with the dividing nucleus. J. Cell Biol. 105, 387-395.
76. Vesk, P.A., Rayns, D.G. & Vesk, M. (1994) Imaging of plant microtubules with high resolution scanning electron microscopy. Protoplasma, 182, 71-74.
77. Wang, H., Cutler, A.J., Saleem, M. & Fowke, L.C. (1989) Microtubules in maize protoplasts derived from cell suspension cultures: effect of calcium and magnesium ions. Eur. J. Cell Biol. 49, 80-86.
78. Wasteneys, G.O., Gunning, B.E.S. & Hepler, P.K. (1993) Microinjection of fluorescent brain tubulin reveals dynamic properties of cortical microtubules in living plant cells. Cell Motil. Cytoskel. 24, 205-213.
79. Weisenberg, R.C. (1972) Microtubule formation in vitro in solutions containing low calcium concentrations. Science, 177, 1104-1105.
80. White, R.G., Hyde, G.J. & Overall, R.L. (1990) Microtubule arrays in regenerating Mougeotia protoplasts may be oriented by electric fields. Protoplasma, 158, 73-85.
81. Williamson, R.E. (1990) Alignment of cortical microtubules by anisotropic wall stresses. Aust. J. Plant Physiol. 17, 601-613.
82. Williamson, R.E. (1991) Orientation of cortical microtubules in interphase plant cells. Int. Rev. Cytol. 129, 135-206.
83. Wymer, C.L., Wymer, S.A., Cosgrove, D.J. & Cyr, R.J. (1995) Plant cell growth responds to external forces and the response is transduced by microtubules. Plant Phys. (in press).
84. Yuan, M., Shaw, P.J., Warn, R.M. & Lloyd, C.W. (1994) Dynamic reorientation of cortical microtubules, from transverse to longitudinal, in living plant cells. Proc. Natl. Acad. Sci 91, 6050-6053.
85. Yuan, M., Warn, R.M., Shaw, P.J. & Lloyd, C.W. (1995) Dynamic microtubules under the radial and outer tangential walls of microinjected pea epidermal cells observed by computer reconstruction. Plant J. 7, 17-23.
86. Zandomeni, K. & Schopfer, P. (1993) Re-orientation of microtubules at the outer epidermal wall of maize coleoptiles by phytochrome, blue-light photoreceptor, and auxin. Protoplasma, 173, 103-112.
87. Zandomeni, K. & Schopfer, P. (1994) Mechanosensory microtubule reorientation in the epidermis of maize coleoptiles subjected to bending stress. Protoplasma, 182, 96-101.
88. Zhang, D.H., Callaham, D.A. & Hepler, P.K. (1990a) Regulation of anaphase chromosome motion in Tradescantia stamen hair cells by calcium and related signaling agents. J. Cell Biol. 111, 171-182.
89. Zhang, D.H., Wadsworth, P. & Hepler, P.K. (1990b) Microtubule dynamics in living dividing plant cells: Confocal imaging of microinjected fluorescent brain tubulin. Proc. Natl. Acad. Sci. 87, 8820-8824.
90. Zhang, D.H., Wadsworth, P. & Hepler, P.K. (1992) Modulation of anaphase spindle microtubule structure in stamen hair cells of Tradescantia by calcium and related agents. J. Cell Sci. 102, 79-89.
91. Zhang, D.H., Wadsworth, P. & Hepler, P.K. (1993) Dynamics of microfilaments are similar, but distinct from microtubules during cytokinesis in living, dividing plant cells. Cell Motil. Cytoskel. 24, 151-155.