Mutation or drug-dependent microtubule disruption causes radial swelling without altering parallel cellulose microfibril deposition in Arabidopsis root cells

Plant Cell

Volumn 15, Issue 6, 2003, Pages 1414-1429

  Sugimoto, Keiko ^a,b   Himmelspach, Regina ^a   Williamson, Richard E ^a   Wasteneys, Geoffrey O ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^b JOHN INNES CENTRE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANISOTROPY; DRUG PRODUCTS; MUTAGENESIS; SWELLING;

MICROFIBRILS;

PLANT CELL CULTURE;

ARABIDOPSIS;

EID: 0038118640     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.011593     Document Type: Article

References (64)

1. Andeme-Onzighi, C., Sivaguru, M., Judy-March, J., Baskin, T.I., and Driouich, A. (2002). The reb1-1 mutation of Arabidopsis alters the morphology of trichoblasts, the expression of arabinogalactan-proteins and the organization of cortical microtubules. Planta 215, 949-958.
2. Arioli, T., et al. (1998). Molecular analysis of cellulose biosynthesis in Arabidopsis. Science 279, 717-720.
3. Baskin, T.I. (2001). On the alignment of cellulose microfibrils by cortical microtubules: A review and a model. Protoplasma 215, 150-171.
4. Baskin, T.I., Wilson, J.E., Cork, A., and Williamson, R.E. (1994). Morphology and microtubule organization in Arabidopsis roots exposed to oryzalin or taxol. Plant Cell Physiol. 35, 935-942.
5. Bichet, A., Desnos, T., Turner, S., Grandjean, O., and Hofte, H. (2001). BOTERO1 is required for normal orientation of cortical microtubules and anisotropic cell expansion in Arabidopsis. Plant J. 25, 137-148.
6. Bokros, C.L., Hugdahl, J.D., Hanesworth, V.R., Murthy, J.V., and Morejohn, L.C. (1993). Characterization of the reversible taxol-induced polymerization of plant tubulin into microtubules. Biochemistry 32, 3437-3447.
7. Burk, D.H., Liu, B., Zhong, R.Q., Morrison, W.H., and Ye, Z.H. (2001). A katanin-like protein regulates normal cell wall biosynthesis and cell elongation. Plant Cell 13, 807-827.
8. Burk, D.H., and Ye, Z.H. (2002). Alteration of oriented deposition of cellulose microfibrils by mutation of a katanin-like microtubule-severing protein. Plant Cell 14, 2145-2160.
9. Burn, J.E., Hocart, C.H., Birch, R.J., Cork, A.C., and Williamson, R.E. (2002). Functional analysis of the cellulose synthase genes CesA1, CesA2, and CesA3 in Arabidopsis. Plant Physiol. 129, 797-807.
10. Camilleri, C., Azimzadeh, J., Pastuglia, M., Bellini, C., Grandjean, O., and Bouchez, D. (2002). The Arabidopsis TONNEAU2 gene encodes a putative novel protein phosphatase 2A regulatory subunit essential for the control of the cortical cytoskeleton. Plant Cell 14, 833-845.
11. Carpita, N.C., and Gibeaut, D.M. (1993). Structural models of primary cell walls in flowering plants: Consistency of molecular structure with the physical properties of the walls during growth. Plant J. 3, 1-30.
12. Chanliaud, E., Burrows, K.M., Jeronimidis, G., and Gidley, M.J. (2002). Mechanical properties of primary plant cell wall analogues. Planta 215, 989-996.
13. Chanliaud, E., and Gidley, M.J. (1999). In vitro synthesis and properties of pectin/Acetobacter xylinus cellulose composites. Plant J. 20, 25-35.
14. Emons, A.M.C., and Mulder, B.M. (1998). The making of the architecture of the plant cell wall: How cells exploit geometry. Proc. Natl. Acad. Sci. USA 95, 7215-7219.
15. Emons, A.M.C., and Mulder, B.M. (2000). How the deposition of cellulose microfibrils builds cell wall architecture. Trends Plant Sci. 5, 35-40.
16. Fagard, M., Desnos, T., Desprez, T., Goubet, F., Refregier, G., Mouille, G., McCann, M., Rayon, C., Vernhettes, S., and Hofte, H. (2000). PROCUSTE1 encodes a cellulose synthase required for normal cell elongation specifically in roots and dark-grown hypocotyls of Arabidopsis. Plant Cell 12, 2409-2423.
17. Fisher, D.D., and Cyr, R.J. (1998). Extending the microtubule/ microfibril paradigm: Cellulose synthesis is required for normal cortical microtubule alignment in elongating cells. Plant Physiol. 116, 1043-1051.
18. Frei, E., and Preston, R.D. (1961). Cell wall organization and wall growth in the filamentous green algae Cladophora and Chaetomorpha. II Spiral growth and spiral structure. Proc. R. Soc. Bot. 155, 55-81.
19. Furutani, I., Watanabe, Y., Prieto, R., Masukawa, M., Suzuki, K., Naoi, K., Thitamadee, S., Shikanai, T., and Hashimoto, T. (2000). The SPIRAL genes are required for directional control of cell elongation in Arabidopsis thaliana. Development 127, 4443-4453.
20. Giddings, T.H., and Staehelin, L.A. (1991). Microtubule-mediated control of microfibril deposition: A re-examination of the hypothesis. In The Cytoskeletal Basis of Plant Growth and Form, C.W. Lloyd, ed (San Diego, CA: Academic Press), pp. 85-100.
21. Gillmor, C.S., Poindexter, P., Lorieau, J., Palcic, M.M., and Somerville, C. (2002). α-Glucosidase I is required for cellulose biosynthesis and morphogenesis in Arabidopsis. J. Cell Biol. 156, 1003-1013.
22. Green, P.B. (1980). Organogenesis, a biophysical view. Annu. Rev. Plant Physiol. 31, 51-82.
23. Hashimoto, T. (2002). Molecular genetic analysis of left-right handedness in plants. Philos. Trans. R. Soc. Lond. B Biol. Sci. 357, 799-808.
24. Hussey, P.J., Hawkins, T.J., Igarashi, H., Kaloriti, D., and Smertenko, A. (2002). The plant cytoskeleton: Recent advances in the study of the plant microtubule-associated proteins MAP-65, MAP-190 and the Xenopus MAP215-like protein, MOR1. Plant Mol. Biol. 50, 915-924.
25. Itoh, T. (1976). Microfibrillar orientation of radially enlarged cells of coumarin- and colchicine-treated pine seedlings. Plant Cell Physiol. 17, 385-398.
26. Itoh, T., and Shimeji, K. (1976). Orientation of microfibrils and microtubules in cortical parenchyma cells of poplar during elongation growth. Bot. Mag. Tokyo 89, 291-308.
27. Lane, D.R., et al. (2001). Temperature-sensitive alleles of RSW2 link the KORRIGAN endo-1,4-β-glucanase to cellulose synthesis and cytokinesis in Arabidopsis. Plant Physiol. 126, 278-288.
28. w and yield of cellulose of the alga Valonia in the presence of colchicine. Biochim. Biophys. Acta 237, 75-77.
29. McCartney, L., Steele-King, C.G., Jordan, E., and Knox, J.P. (2003). Cell wall pectic (1→4)-β-D-galactan marks the acceleration of cell elongation in the Arabidopsis seedling root meristem. Plant J. 33, 447-454.
30. Morejohn, L.C., and Fosket, D.E. (1991). The biochemistry of compounds with anti-microtubule activity in plant cells. Pharmacol. Ther. 51, 217-230.
31. Mueller, S.C., and Brown, R.M. (1982). The control of cellulose microfibril deposition in the cell wall of higher plants. II. Freeze-fracture microfibril patterns in maize seedling tissues following experimental alteration with colchicine and ethylene. Planta 154, 501-515.
32. Mulder, B.M., and Emons, A.M.C. (2001). A dynamical model for plant cell wall architecture formation. J. Math. Biol. 42, 261-289.
33. Nicol, F., His, I., Jauneau, A., Vernhettes, S., Canut, H., and Hofte, H. (1998). A plasma membrane-bound putative endo-1,4-β-D-glucanase is required for normal wall assembly and cell elongation in Arabidopsis. EMBO J. 17, 5563-5576.
34. Okuda, K., and Mizuta, S. (1987). Modification in cell shape unrelated to cellulose microfibril orientation in growing thallus cells of Chaetomorpha moniligera. Plant Cell Physiol. 28, 461-473.
35. O'Neill, M.A., Eberhard, S., Albersheim, P., and Darvill, A.G. (2001). Requirement of borate cross-linking of cell wall rhamnogalacturonan II for Arabidopsis growth. Science 294, 846-849.
36. Pagant, S., Bichet, A., Sugimoto, K., Lerouxel, O., Desprez, T., McCann, M., Lerouge, P., Vernhettes, S., and Hofte, H. (2002). KOBITO1 encodes a novel plasma membrane protein necessary for normal synthesis of cellulose during cell expansion in Arabidopsis. Plant Cell 14, 2001-2013.
37. Peng, L.C., Hocart, C.H., Redmond, J.W., and Williamson, R.E. (2000). Fractionation of carbohydrates in Arabidopsis root cell walls shows that three radial swelling loci are specifically involved in cellulose production. Planta 211, 406-414.
38. Probine, M.C. (1963). Cell growth and the structure and mechanical properties of the wall in internodal cells of Nitella opaca. III. Spiral growth and cell wall structure. J. Exp. Bot. 14, 101-113.
39. Sato, S., Kato, T., Kakegawa, K., Ishii, T., Liu, Y.G., Awano, T., Takabe, K., Nishiyama, Y., Kuga, S., Nakamura, Y., Tabata, S., and Shibata, D. (2001). Role of the putative membrane-bound endo-1,4-β-glucanase KORRIGAN in cell elongation and cellulose synthesis in Arabidopsis thaliana. Plant Cell Physiol. 42, 251-263.
40. Seifert, G.J., Barber, C., Wells, B., Dolan, L., and Roberts, K. (2002). Galactose biosynthesis in Arabidopsis: Genetic evidence for substrate channeling from UDP-D-galactose into cell wall polymers. Curr. Biol. 12, 1840-1845.
41. Shibaoka, H., and Hogetsu, T. (1977). Effects of ethyl N-phenylcarbamate on wall microtubules and on gibberellin- and kinetin-controlled cell expansion. Bot. Mag. Tokyo 90, 317-321.
42. Srivastava, L.M., Sawhney, V.K., and Bonnettemaker, M. (1976). Cell growth, wall deposition, and correlated fine structure of colchicine-treated lettuce hypocotyl cells. Can. J. Bot. 55, 902-917.
43. Steinborn, K., Maulbetsch, C., Priester, B., Trautmann, S., Pacher, T., Geiges, B., Kuttner, F., Lepiniec, L., Stierhof, Y.D., Schwarz, H., Jurgens, G., and Mayer, U. (2002). The Arabidopsis PILZ group genes encode tubulin-folding cofactor orthologs required for cell division but not cell growth. Genes Dev. 16, 959-971.
44. Sugimoto, K., Williamson, R.E., and Wasteneys, G.O. (2000). New techniques enable comparative analysis of microtubule orientation, wall texture, and growth rate in intact roots of Arabidopsis. Plant Physiol. 124, 1493-1506.
45. Sugimoto, K., Williamson, R.E., and Wasteneys, G.O. (2001). Wall architecture in the cellulose-deficient rsw1 mutant of Arabidopsis thaliana: Microfibrils but not microtubules lose their transverse alignment before microfibrils become unrecognizable in the mitotic and elongation zones of roots. Protoplasma 215, 172-183.
46. Taiz, L. (1984). Plant-cell expansion: Regulation of cell-wall mechanical properties. Annu. Rev. Plant Physiol. Plant Mol. Biol. 35, 585-657.
47. Takeda, K., and Shibaoka, H. (1981). Effects of gibberellin and colchicine on microfibril arrangement in epidermal cell walls of Vigna angularis Ohwi et Ohashi epicotyls. Planta 151, 393-398.
48. Thitamadee, S., Tuchihara, K., and Hashimoto, T. (2002). Microtubule basis for left-handed helical growth in Arabidopsis. Nature 417, 193-196.
49. Traas, J., Bellini, C., Nacry, P., Kronenberger, J., Bouchez, D., and Caboche, M. (1995). Normal differentiation patterns in plants lacking microtubular preprophase bands. Nature 375, 676-677.
50. Wasteneys, G.O. (2000). The cytoskeleton and growth polarity. Curr. Opin. Plant Biol. 3, 503-511.
51. Wasteneys, G.O. (2002). Microtubule organization in the green kingdom: Chaos or self-order? J. Cell Sci. 115, 1345-1354.
52. Wasteneys, G.O., and Williamson, R.E. (1987). Microtubule orientation in developing internodal cells of Nitella: A quantitative analysis. Eur. J. Cell Biol. 43, 14-22.
53. Webb, M., Jouannic, S., Foreman, J., Linstead, P., and Dolan, L. (2002). Cell specification in the Arabidopsis root epidermis requires the activity of ECTOPIC ROOT HAIR 3, a katanin-p60 protein. Development 129, 123-131.
54. Weedenburg, C.A., and Seagull, R.W. (1987). The effects of taxol and colchicine on microtubule and microfibril arrays in elongating plant cells in culture. Can. J. Bot. 66, 1707-1716.
55. Whitney, S.E.C., Brigham, J.E., Darke, A.H., Reid, J.S.G., and Gidley, M.J. (1995). In vitro assembly of cellulose/xyloglucan networks: Ultrastructural and molecular aspects. Plant J. 8, 491-504.
56. Whitney, S.E.C., Gothard, M.G.E., Mitchell, J.T., and Gidley, M.J. (1999). Roles of cellulose and xyloglucan in determining the mechanical properties of primary plant cell walls. Plant Physiol. 121, 657-663.
57. Whittington, A.T., Vugrek, O., Wei, K.J., Hasenbein, N.G., Sugimoto, K., Rashbrooke, M.C., and Wasteneys, G.O. (2001). MOR1 is essential for organizing cortical microtubules in plants. Nature 411, 610-613.
58. Wiedemeier, A.M.D., Judy-March, J.E., Hocart, C.H., Wasteneys, G.O., Williamson, R.E., and Baskin, T.I. (2002). Mutant alleles of Arabidopsis RADIALLY SWOLLEN 4 and 7 reduce growth anisotropy without altering the transverse orientation of cortical microtubules or cellulose microfibrils. Development 129, 4821-4830.
59. Williamson, R.E., Burn, J.E., and Hocart, C.H. (2001). Cellulose synthesis: Mutational analysis and genomic perspectives using Arabidopsis thaliana. Cell. Mol. Life Sci. 58, 1475-1490.
60. Wilms, F.H.A., Wolters-Arts, A.M.C., and Derksen, J. (1990). Orientation of cellulose microfibrils in cortical cells of tobacco explants. Effects of microtubule-depolymerizing drugs. Planta 182, 1-8.
61. Wilson, R.H., Smith, A.C., Kacurakova, M., Saunders, P.K., Wellner, N., and Waldron, K.W. (2000). The mechanical properties and molecular dynamics of plant cell wall polysaccharides studied by Fourier-transform infrared spectroscopy. Plant Physiol. 124, 397-405.
62. Yasuhara, H., Muraoka, M., Shogaki, H., Mori, H., and Sonobe, S. (2002). TMBP200, a microtubule bundling polypeptide isolated from telophase tobacco BY-2 cells, is a MOR1 homologue. Plant Cell Physiol. 43, 595-603.
63. Yatsu, L.Y., and Jacks, T.J. (1981). An ultrastructural study of the relationship between microtubules and microfibrils in cotton (Gossypium hirsutum L.) cell-wall reversals. Am. J. Bot. 68, 771-777.
64. Zhong, R.Q., Burk, D.H., Morrison, W.H., and Ye, Z.H. (2002). A kinesin-like protein is essential for oriented deposition of cellulose microfibrils and cell wall strength. Plant Cell 14, 3101-3117.