Arabidopsis SPIRAL2 promotes uninterrupted microtubule growth by suppressing the pause state of microtubule dynamics

Journal of Cell Science

Volumn 121, Issue 14, 2008, Pages 2372-2381

  Yao, Maki ^a   Wakamatsu, Yoshinori ^a   Itoh, Tomohiko J ^b   Shoji, Tsubasa ^a   Hashimoto, Takashi ^a  

^a NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^b NAGOYA UNIVERSITY   (Japan)

Author keywords

Arabidopsis thaliana; HEAT repeats; MAP; Microtubule; Pause; SPIRAL2

Indexed keywords

ARABIDOPSIS PROTEIN; BINDING PROTEIN; END BINDING 1 PROTEIN; GREEN FLUORESCENT PROTEIN; MICROTUBULE ASSOCIATED PROTEIN 2; PROTEIN HEAT; PROTEIN SP2L; PROTEIN SPIRAL 2; VEGETABLE PROTEIN;

AMINO TERMINAL SEQUENCE; ARABIDOPSIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL GROWTH; CELL KINETICS; CONTROLLED STUDY; ENZYME REPRESSION; GENE FUSION; IN VITRO STUDY; MICROTUBULE ASSEMBLY; MUTANT; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENE EXPRESSION REGULATION, PLANT; GREEN FLUORESCENT PROTEINS; HYPOCOTYL; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; PROTEIN BINDING; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; SEEDLING;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 49649104566     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.030221     Document Type: Article

References (42)

1. Abe, T. and Hashimoto, T. (2005). Altered microtubule dynamics by expression of modified α-tubulin protein causes right-handed helical growth in transgenic Arabidopsis plants. Plant J. 43: 191-204.
2. Akhmanova, A. and Steinmetz, M. O. (2008). Tracking the ends: a dynamic protein network controls the fate of microtubule tips. Nat. Rev. Mol. Cell Biol. 9, 309-322.
3. Al-Bassam, J., Larsen, N. A., Hyman, A. A. and Harrison, S. C. (2007). Crystal structure of a TOG domain: conserved features of XMAP215/ Dis1 -family TOG domains and implications for tubulin binding. Structure 15, 355-362.
4. Ambrose, J. C., Shoji, T., Kotzer, A. M., Pighin, J. A. and Wasteneys, G. O. (2007). The Arabidopsis CLASP gene encodes a microtubule-associated protein involved in cell expansion and division. Plant Cell 19, 2763-2775.
5. Arnal, I., Karsenti, E. and Hyman, A. A. (2000). Structural transitions at microtubule ends correlate with their dynamic properties in Xenopus egg extracts. J. Cell Biol. 149, 767-774.
6. Bieling, P., Laan, L., Schek, H., Munteanu, E. L., Sandblad, L., Dogterom, M., Brunner, D. and Surrey, T. (2007). Reconstitution of a microtubule plus-end tracking system in vitro. Nature 450, 1100-1105.
7. Bisgrove, S. R., Hable, W. E. and Kropf, D. L. (2004). +TlPs and microtubule regulation. The beginning of the plus end in plants. Plant Physiol. 136, 3855-3863.
8. Brittle, A. and Ohkura, H. (2005). Mini spindles, the XMAP215 homologue, suppresses pausing of interphase microtubules in Drosophila. EMBO J. 24, 1387-1396.
9. Brouhard, G. J., Stear, J. H., Noetzel, T. L., Al-Bassam, J., Kinoshita, K., Harrison, S. C., Howard, J. and Hyman, A. A. (2008). XMAP215 is a processive microtubule polymerase. Cell 132, 79-88.
10. Buschmann, H., Fabri, C. O., Hauptmann, M., Hutzler, P., Laux, T., Lloyd, C. W. and Schäffner, A. R. (2004). Helical growth of the Arabidopsis mutant tortifolia1 reveals a plant-specific microtubule-associated protein. Curr. Biol. 14, 1515-1521.
11. Chan, J., Calder, G., Fox, S. and Lloyd, C. (2007). Cortical microtubule arrays undergo rotary movements in Arabidopsis hypocotyl epidermal cells. Nat. Cell Biol. 9, 171-175.
12. Clough, S. J. and Bent, A. F. (1998). Floral dip: a simplified method for Agrobacterium mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
13. Crawford, K. M. and Zambryski, P. C. (2000). Subcellular localization determines the availability of non-targeted proteins to plasmodesmatal transport. Curr. Biol. 10, 1032-1040.
14. Desai, A. and Mitchison, T. J. (1997). Microtubule polymerization dynamics. Annu. Rev. Cell Dev. Biol. 13, 83-117.
15. Dixit, R. and Cyr, R. (2004). Encounters between dynamic cortical microtubules promote ordering of the cortical array through angle-dependent modifications of microtubule behavior. Plant Cell 16, 3274-3284.
16. 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.
17. Gard, D. L. and Kirschner, M. W. (1987). Microtubule assembly in cytoplasmic extracts of Xenopus oocytes and eggs. J. Cell Biol. 105, 2191-2201.
18. Gardiner, J. and Marc, J. (2003). Putative microtubule-associated proteins from the Arabidopsis genome. Protoplasma 222, 61-74.
19. Grego, S., Cantillana, V. and Saimon, E. D. (2001). Microtubule treadmilling in vitro investigated by fluorescence speckle and confocal microscopy. Biophys. J. 81, 66-78.
20. Hamada, T., Igarashi, H., Itoh, T. J., Shimmen, T. and Sonobe, S. (2004). Characterization of a 200 kDa microtubule-associated protein of tobacco BY-2 cells, a member of the XMAP216/MOR1 family. Plant Cell Physiol. 45, 1233-1242.
21. Ishida, T., Kaneko, Y., Iwano, M. and Hashimoto, T. (2007). Helical microtubule arrays in a collection of twisting tubulin mutants of Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 104, 8544-8549.
22. Itoh, T. J., Hisanaga, S., Hosoi, T., Kishimoto, T. and Hotani, H. (1997). Phosphorylation states of microtubule-associated protein 2 (MAP2) determine the regulatory role of MAP2 in microtubule dynamics. Biochemistry 36, 12574-12582.
23. Kawamura, E., Himmelspach, R., Rashbrooke, M. C., Whittington, A. T., Gale, K. R., Collings, D. A. and Wasteneys, G. O. (2006). MICROTUBULE ORGANIZATION 1 regulates structure and function of microtubule arrays during mitosis and cytokinesis in the Arabidopsis root. Plant Physiol. 140, 102-114.
24. Kirik, V., Herrmann, U., Parupalli, C., Sedbrook, J. C., Ehrhardt, D. W. and Hülskamp, M. (2007). CLASP localizes in two discrete patterns on cortical microtubules and is required for cell morphogenesis and cell division in Arabidopsis. J. Cell Sci. 120, 4416-4425.
25. Moore, R. C., Zhang, M., Cassimeris, L. and Cyr, R. J. (1997). In vitro assembled plant microtubules exhibit a high state of dynamic instability. Cell Motil. Cytoskeleton 38, 278-286.
26. Nakagawa, T., Kurose, T., Hino, T., Tanaka, K., Kawamukai, M., Niwa, Y., Toyooka, K., Matsuoka, K., Jinbo, T. and Kimura, T. (2007). Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J. Biosci. Bioeng. 104, 34-41.
27. Nakajima, K., Furutani, I., Tachimoto, H., Matsubara, K. and Hashimoto, T. (2004). SPIRAL1 encodes a plant-specific microtubule-localized protein required for directional control of rapidly expanding Arabidopsis cells. Plant Cell 16, 1178-1190.
28. Nakamura, M., Naoi, K., Shoji, T. and Hashimoto, T. (2004). Low concentrations of propyzamide and oryzalin alter microtubule dynamics in Arabidopsis epidermal cells. Plant Cell Physiol. 45, 1330-1334.
29. Nakao, C., Itoh, T. J., Hotani, H. and Mori, N. (2004). Modulation of the stathmin-like microtubule destabilizing activity of RB3, a neuron-specific member of the SCG10 family, by its N-terminal domain. J. Biol. Chem. 279, 23014-23021.
30. Rusan, N. M., Fagerstrom, C. J., Yvon, A. M. and Wadsworth, P. (2001). Cell cycle-dependent changes in microtubule dynamics in living cells expressing green fluorescent protein-α tubulin. Mol. Biol. Cell 12, 971-980.
31. Schek, H. T., III, Gardner, M. K., Cheng, J., Odde, D. J. and Hunt, A. J. (2007). Microtubule assembly dynamics at the nanoscale. Curr. Biol. 17, 1445-1455.
32. Sedbrook, J. C., Ehrhardt, D. W., Fisher, S. E., Scheible, W. R. and Somerville, C. R. (2004). The Arabidopsis sku6/spiral1 gene encodes a plus end-localized microtubule-interacting protein involved in directional cell expansion. Plant Cell 16, 1506-1520.
33. Shaw, S. L., Kamyar, R. and Ehrhardt, D. W. (2003). Sustained microtubule treadmilling in Arabidopsis cortical arrays. Science 300, 1715-1718.
34. Shirasu-Hiza, M., Coughlin, P. and Mitchison, T. (2003). Identification of XMAP215 as a microtubule-destabilizing factor in Xenopus egg extract by biochemical purification. J. Cell Biol. 161, 349-358.
35. Shoji, T., Narita, N. N., Hayashi, K., Asada, J., Hamada, T., Sonobe, S., Nakajima, K. and Hashimoto, T. (2004). Plant-specific microtubule-associated protein SPIRAL2 is required for anisotropic growth in Arabidopsis. Plant Physiol. 136, 3933-3944.
36. Slep, K. C. and Vale, R. D. (2007). Structural basis of microtubule plus end tracking by XMAP215, CLIP-170, and EB1. Mol. Cell 27, 976-991.
37. Tirnauer, J. S., Grego, S., Salmon, E. D. and Mitchison, T. J. (2002). EB1-microtubule interactions in Xenopus egg extracts: role of EB1 in microtubule stabilization and mechanisms of targeting to microtubules. Mol. Biol. Cell 13, 3614-3626.
38. Toso, R. J., Jordan, M. A., Farrell, K. W., Matsumoto, B. and Wilson, L. (1993). Kinetic stabilization of microtubule dynamic instability in vitro by vinblastine. Biochemistry 32, 1285-1293.
39. Tran, P. T., Walker, R. A. and Salmon, E. D. (1997). A metastable intermediate state of microtubule dynamic instability that differs significantly between plus and minus ends. J. Cell Biol. 138, 105-117.
40. 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.
41. Vos, J. W., Dogterom, M. and Emons, A. M. (2004). Microtubules become more dynamic but not shorter during preprophase band formation: a possible "search-and-capture" mechanism for microtubule translocation. Cell Motil. Cytoskeleton 57, 246-258.
42. Zimmermann, P., Hirsch-Hoffmann, M., Henning, L. and Gruissem, W. (2004). GENEVESTIGATOR: Arabidopsis thaliana microarray database and analysis toolbox. Plant Physiol. 136, 2621-2632.