γ-tubulin is essential for microtubule organization and development of Arabidopsis

Plant Cell

Volumn 18, Issue 6, 2006, Pages 1412-1425

  Pastuglia, Martine ^a   Azimzadeh, Juliette ^a,b   Goussot, Magali ^a   Camilleri, Christine ^a   Belcram, Katia ^a   Evrard, Jean Luc ^b   Schmit, Anne Catherine ^b   Guerche, Philippe ^a   Bouchez, David ^a  

^a CEMAGREF   (France)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; GENES; GENETIC ENGINEERING; NUCLEATION; PROTEINS;

ARABIDOPSIS THALIANA; GAMETOPHYTES; GAMMA-TUBULIN GENES; MICROTUBULE ARRAYS;

PLANTS (BOTANY);

CELLS; GENES; GENETIC ENGINEERING; NUCLEATION; PLANTS; PROTEINS;

ANIMALIA; ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 33745432088     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.105.039644     Document Type: Article

References (61)

1. Alexander, M.P. (1969). Differential staining of aborted and non aborted pollen. Stain Technol. 44, 117-122.
2. Alonso, J.M., et al. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301, 653-657.
3. Arabidopsis Genome Initiative (2000). Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796-815.
4. Azimzadeh, J., Traas, J., and Pastuglia, M. (2001). Molecular aspects of microtubule dynamics in plants. Curr. Opin. Plant Biol. 4, 513-519.
5. Baluska, F., Hlavacka, A., Samaj, J., Palme, K., Robinson, D.G., Matoh, T., McCurdy, D.W., Menzel, D., and Volkmann, D. (2002). F-actin-dependent endocytosis of cell wall pectins in meristematic root cells. Insights from brefeldin A-induced compartments. Plant Physiol. 130, 422-431.
6. Bao, Y., Kost, B., and Chua, N.H. (2001). Reduced expression of alpha-tubulin genes in Arabidopsis thaliana specifically affects root growth and morphology, root hair development and root gravitropism. Plant J. 28, 145-157.
7. Barton, M.K., and Poethig, R.S. (1993). Formation of the shoot apical meristem in Arabidopsis thaliana: An analysis of development in the wild type and in the shoot meristemless mutant. Development 119, 823-831.
8. 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.
9. Bechtold, H., Ellis, J., and Pelletier, G. (1993). In planta Agrobacterium mediated gene transfer by infiltration of adult Arabidopsis thaliana plants. C. R. Acad. Sci. Paris 316, 1194-1199.
10. Bouchez, D., Camilleri, C., and Caboche, M. (1993). A binary vector based on Basta resistance for in planta transformation of Arabidopsis thaliana. C. R. Acad. Sci. Paris 316, 1188-1193.
11. Brown, R.C., Lemmon, B.E., and Horio, T. (2004). Gamma-tubulin localization changes from discrete polar organizers to anastral spindles and phragmoplasts in mitosis of Marchantia polymorpha L. Protoplasma 224, 187-193.
12. Camilleri, C., Azimzadeh, J., Pastuglia, M., Bellini, C., Grandjean, O., and Bouchez, D. (2002). The Arabidopsis TONNEAU2 gene encodes a putative novel PP2A regulatory subunit essential for the control of cortical cytoskeleton. Plant Cell 14, 833-845.
13. Chan, J., Calder, G.M., Doonan, J.H., and Lloyd, C.W. (2003). EB1 reveals mobile microtubule nucleation sites in Arabidopsis. Nat. Cell Biol. 5, 967-971.
14. Christensen, C.A., King, E.J., Jordan, J.R., and Drews, G.N. (1997). Megagametogenesis in Arabidopsis wild type and the Gf mutant. Sex. Plant Reprod. 10, 49-64.
15. Christensen, C.A., Subramanian, S., and Drews, G.N. (1998). Identification of gametophytic mutations affecting female gametophyte development in Arabidopsis. Dev. Biol. 202, 136-151.
16. Derksen, J., Knuiman, B., Hoedemaekers, K., Guyon, A., Bonhomme, S., and Pierson, E.S. (2002). Growth and cellular organization of Arabidopsis pollen tubes in vitro. Sex. Plant Reprod. 15, 133-139.
17. Dolan, L., Janmaat, K., Willemsen, V., Linstead, P., Poethig, S., Roberts, K., and Scheres, B. (1993). Cellular organisation of the Arabidopsis thaliana root. Development 119, 71-84.
18. Drykova, D., Cenklova, V., Sulimenko, V., Volc, J., Draber, P., and Binarova, P. (2003). Plant gamma-tubulin interacts with alpha beta-tubulin dimers and forms membrane-associated complexes. Plant Cell 15, 465-480.
19. Erhardt, M., Stoppin-Mellet, V., Campagne, S., Canaday, J., Mutterer, J., Fabian, T., Sauter, M., Muller, T., Peter, C., Lambert, A.M., and Schmit, A.C. (2002). The plant Spc98p homologue colocalizes with gamma-tubulin at microtubule nucleation sites and is required for microtubule nucleation. J. Cell Sci. 115, 2423-2431.
20. Evrard, J.L., Nguyen, I., Bergdoll, M., Mutterer, J., Steinmetz, A., and Lambert, A.M. (2002). A novel pollen-specific alpha-tubulin in sunflower: Structure and characterization. Plant Mol. Biol. 49, 611-620.
21. Hendrickson, T.W., Yao, J., Bhadury, S., Corbett, A.H., and Joshi, H.C. (2001). Conditional mutations in gamma-tubulin reveal its involvement in chromosome segregation and cytokinesis. Mol. Biol. Cell 12, 2469-2481.
22. Horio, T., and Oakley, B.R. (2003). Expression of Arabidopsis gamma-tubulin in fission yeast reveals conserved and novel functions of gamma-tubulin. Plant Physiol. 133, 1926-1934.
23. Horio, T., Uzawa, S., Jung, M.K., Oakley, B.R., Tanaka, K., and Yanagida, M. (1991). The fission yeast gamma-tubulin is essential for mitosis and is localized at microtubule organizing centers. J. Cell Sci. 99, 693-700.
24. Jaspersen, S.L., and Winey, M. (2004). The budding yeast spindle pole body: Structure, duplication, and function. Annu. Rev. Cell Dev. Biol. 20, 1-28.
25. Jeng, R., and Stearns, T. (1999). Gamma-tubulin complexes: Size does matter. Trends Cell Biol. 9, 339-342.
26. Job, D., Valiron, O., and Oakley, B. (2003). Microtubule nucleation. Curr. Opin. Cell Biol. 15, 111-117.
27. Joshi, H.C., and Palevitz, B.A. (1996). Gamma-tubulin and microtubule organization in plants. Trends Cell Biol. 6, 41-44.
28. Jung, M.K., Prigozhina, N., Oakley, C.E., Nogales, E., and Oakley, B.R. (2001). Alanine-scanning mutagenesis of Aspergillus gamma-tubulin yields diverse and novel phenotypes. Mol. Biol. Cell 12, 2119-2136.
29. Laux, T., Mayer, K.F.X., Berger, J., and Jurgens, G. (1996). The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122, 87-96.
30. Liu, B., Joshi, H.C., Wilson, T.J., Silflow, C.D., Palevitz, B.A., and Snustad, D.P. (1994). Gamma-tubulin in Arabidopsis: Gene sequence, immunoblot, and immunofluorescence studies. Plant Cell 6, 303-314.
31. Liu, B., Marc, J., Joshi, H.C., and Palevitz, B.A. (1993). A gamma-tubulin-related protein associated with the microtubule arrays of higher plants in a cell cycle-dependent manner. J. Cell Sci. 104, 1217-1228.
32. Marc, J., Granger, C.L., Brincat, J., Fisher, D.D., Kao, T.H., McCubbin, A.G., and Cyr, R.J. (1998). A GFP-MAP4 reporter gene for visualizing cortical microtubule rearrangements in living epidermal cells. Plant Cell 10, 1927-1939.
33. Marschall, L.G., Jeng, R.L., Mulholland, J., and Stearns, T. (1996). Analysis of Tub4p, a yeast gamma-tubulin-like protein: Implications for microtubule-organizing center function. J. Cell Biol. 134, 443-454.
34. Martin, M.A., Osmani, S.A., and Oakley, B.R. (1997). The role of gamma-tubulin in mitotic spindle formation and cell cycle progression in Aspergillus nidulans. J. Cell Sci. 110, 623-633.
35. Moffatt, B.A., McWhinnie, E.A., Agarwal, S.K., and Schaff, D.A. (1994). The adenine phosphoribosyltransferase-encoding gene of Arabidopsis thaliana. Gene 143, 211-216.
36. Moritz, M., and Agard, D.A. (2001). Gamma-tubulin complexes and microtubule nucleation. Curr. Opin. Struct. Biol. 11, 174-181.
37. Moussian, B., Schoof, H., Haecker, A., Jurgens, G., and Laux, T. (1998). Role of the ZWILLE gene in the regulation of central shoot meristem cell fate during Arabidopsis embryogenesis. EMBO J. 17, 1799-1809.
38. Murata, T., Sonobe, S., Baskin, T.I., Hyodo, S., Hasezawa, S., Nagata, T., Horio, T., and Hasebe, M. (2005). Microtubule-dependent microtubule nucleation based on recruitment of gamma-tubulin in higher plants. Nat. Cell Biol. 7, 961-968.
39. Nacry, P., Camilleri, C., Courtial, B., Caboche, M., and Bouchez, D. (1998). Major chromosomal rearrangements induced by T-DNA transformation in Arabidopsis. Genetics 149, 641-650.
40. Oakley, B.R., Oakley, C.E., Yoon, Y.S., and Jung, M.K. (1990). Gamma-tubulin is a component of the spindle pole body that is essential for microtubule function in Aspergillus nidulans. Cell 61, 1289-1301.
41. Paluh, J.L., Nogales, E., Oakley, B.R., McDonald, K., Pidoux, A.L., and Cande, W.Z. (2000). A mutation in gamma-tubulin alters microtubule dynamics and organization and is synthetically lethal with the kinesin-like protein Pkl1p. Mol. Biol. Cell 11, 1225-1239.
42. Panteris, E., Apostolakos, P., Graf, R., and Galatis, B. (2000). Gamma-tubulin colocalizes with microtubule arrays and tubulin paracrystals in dividing vegetative cells of higher plants. Protoplasma 210, 179-187.
43. Park, S.K., Howden, R., and Twell, D. (1998). The Arabidopsis thaliana gametophytic mutation gemini pollen1 disrupts microspore polarity, division asymmetry and pollen cell fate. Development 125, 3789-3799.
44. Prigozhina, N.L., Oakley, C.E., Lewis, A.M., Nayak, T., Osmani, S.A., and Oakley, B.R. (2004). Gamma-tubulin plays an essential role in the coordination of mitotic events. Mol. Biol. Cell 15, 1374-1386.
45. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
46. Sampaio, P., Rebollo, E., Varmark, H., Sunkel, C.E., and Gonzalez, C. (2001). Organized microtubule arrays in gamma-tubulin-depleted Drosophila spermatocytes. Curr. Biol. 11, 1788-1793.
47. Shaw, S.L., Kamyar, R., and Ehrhardt, D.W. (2003). Sustained microtubule treadmilling in Arabidopsis cortical arrays. Science 300, 1715-1718.
48. Shimamura, M., Brown, R.C., Lemmon, B.E., Akashi, T., Mizuno, K., Nishihara, N., Tomizawa, K.I., Yoshimoto, K., Deguchi, H., Hosoya, H., Horio, T., and Mineyuki, Y. (2004). Gamma-tubulin in basal land plants: Characterization, localization, and implication in the evolution of acentriolar microtubule organizing centers. Plant Cell 16, 45-59.
49. Sobel, S.G., and Snydeŕ, M. (1995). Highly divergent gamma-tubulin gene is essential for cell growth and proper microtubule organization in Saccharomyces cerevisiae. J. Cell Biol. 131, 1775-1788.
50. Spang, A., Geissler, S., Grein, K., and Schiebel, E. (1996). Gamma-tubulin-like Tub4p of Saccharomyces cerevisiae is associated with the spindle pole body substructures that organize microtubules and is required for mitotic spindle formation. J. Cell Biol. 134, 429-441.
51. Stoppin, V., Vantard, M., Schmit, A.C., and Lambert, A.M. (1994). Isolated plant nuclei nucleate microtubule assembly: The nuclear surface in higher plants has centrosome-like activity. Plant Cell 6, 1099-1106.
52. Stoppin-Mellet, V., Peter, C., and Lambert, A.M. (2000). Distribution of gamma-tubulin in higher plant cells: Cytosolic gamma-tubulin is part of high molecular weight complexes. Plant Biol. 2, 290-296.
53. 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.
54. Sunkel, C.E., Gomes, R., Sampaio, P., Perdigao, J., and Gonzalez, C. (1995). Gamma-tubulin is required for the structure and function of the microtubule organizing centre in Drosophila neuroblasts. EMBO J. 14, 28-36.
55. Traas, J., Laufs, P., Julien, M., and Caboche, M. (1995). A mutation affecting etiolation and cell elongation in Nicotiana plumbaginifolia causes abnormal division plane alignment and pattern formation in the root meristem. Plant J. 7, 785-796.
56. Twell, D., Park, S.K., Hawkins, T.J., Schubert, D., Schmidt, R., Smertenko, A., and Hussey, P.J. (2002). MOR1/GEM1 has an essential role in the plant-specific cytokinetic phragmoplast. Nat. Cell Biol. 4, 711-714.
57. Van Bruaene, N., Joss, G., and Van Oostveldt, P. (2004). Reorganization and in vivo dynamics of microtubules during Arabidopsis root hair development. Plant Physiol. 136, 3905-3919.
58. Vogel, J., Drapkin, B., Oomen, J., Beach, D., Bloom, K., and Snyder, M. (2001). Phosphorylation of gamma-tubulin regulates microtubule organization in budding yeast. Dev. Cell 1, 621-631.
59. Wasteneys, G.O. (2002). Microtubule organization in the green kingdom: Chaos or self-order? J. Cell Sci. 115, 1345-1354.
60. 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.
61. Zimmermann, P., Hirsch-Hoffmann, M., Hennig, L., and Gruissem, W. (2004). GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol. 136, 2621-2632.