The γ-tubulin complex protein gcp4 is required for organizing functional microtubule arrays in arabidopsis thaliana

Plant Cell

Volumn 22, Issue 1, 2010, Pages 191-204

  Kong, Zhaosheng ^a   Hotta, Takashi ^a   Julie Lee, Yuh Ru ^a   Horio, Tetsuya ^b   Liu, Bo ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF KANSAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS THALIANA;

EID: 77950345350     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.109.071191     Document Type: Article

References (65)

1. Alvarez, J.P., Pekker, I., Goldshmidt, A., Blum, E., Amsellem, Z., and Eshed, Y. (2006). Endogenous and synthetic microRNAs stimulate simultaneous, efficient, and localized regulation of multiple targets in diverse species. Plant Cell 18: 1134-1151.
2. Ambrose, J.C., Li, W., Marcus, A., Ma, H., and Cyr, R. (2005). A minus-end-directed kinesin with plus-end tracking protein activity is involved in spindle morphogenesis. Mol. Biol. Cell 16: 1584-1592.
3. Anders, A., Lourenco, P.C.C., and Sawin, K.E. (2006). Noncore components of the fission yeast g-tubulin complex. Mol. Biol. Cell 17: 5075-5093.
4. Binarova, P., Cenklova, V., Prochazkova, J., Doskocilova, A., Volc, J., Vrlik, M., and Bogre, L. (2006). g-Tubulin is essential for acentrosomal microtubule nucleation and coordination of late mitotic events in Arabidopsis. Plant Cell 18: 1199-1212.
5. Brown, R.C., and Lemmon, B.E. (2006). Polar organizers and girdling bands of microtubules are associated with gamma-tubulin and act in establishment of meiotic quadripolarity in the hepatic Aneura pinguis (Bryophyta). Protoplasma 227: 77-85.
6. Brown, R.C., and Lemmon, B.E. (2007). The pleiotrophic plant MTOC: an evolutionary perspective. J. Integr. Plant Biol. 49: 1142-1153.
7. Buschmann, H., and Lloyd, C.W. (2008). Arabidopsis mutants and the network of microtubule-associated functions. Mol. Plant 1: 888-898.
8. Chan, J., Sambade, A., Calder, G., and Lloyd, C. (2009). Arabidopsis cortical microtubules are initiated along, as well as branching from, existing microtubules. Plant Cell 21: 2298-2306.
9. Chen, C.B., Marcus, A., Li, W.X., Hu, Y., Calzada, J.P.V., Grossniklaus, U., Cyr, R.J., and Ma, H. (2002). The Arabidopsis ATK1 gene is required for spindle morphogenesis in male meiosis. Development 129: 2401-2409.
10. 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.
11. Czechowski, T., Stitt, M., Altmann, T., Udvardi, M.K., and Scheible, W.R. (2005). Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 139: 5-17.
12. Dixit, R., and Cyr, R. (2004). Encounters between dynamic cortical microtubules promote ordering of the cortical array through angledependent modifications of microtubule behavior. Plant Cell 16: 3274-3284.
13. Earley, K.W., Haag, J.R., Pontes, O., Opper, K., Juehne, T., Song, K.M., and Pikaard, C.S. (2006). Gateway-compatible vectors for plant functional genomics and proteomics. Plant J. 45: 616-629.
14. 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 g-tubulin at microtubule nucleation sites and is required for microtubule nucleation. J. Cell Sci. 115: 2423-2431.
15. Fava, F., Raynaud-Messina, B., Leung-Tack, J., Mazzolini, L., Li, M., Guillemot, J.C., Cachot, D., Tollon, Y., Ferrara, P., and Wright, M. (1999). Human 76p: A new member of the gamma-tubulin-associated protein family. J. Cell Biol. 147: 857-868.
16. Fujita, A., Vardy, L., Garcia, M.A., and Toda, T. (2002). A fourth component of the fission yeast g-tubulin complex, Alp16, is required for cytoplasmic microtubule integrity and becomes indispensable when g-tubulin function is compromised. Mol. Biol. Cell 13: 2360-2373.
17. Guan, K.L., and Dixon, J.E. (1991). Eukaryotic proteins expressed in Escherichia coli: An improved thrombin cleavage and purification procedure of fusion proteins with glutathione S-transferase. Anal. Biochem. 192: 262-267.
18. Gunawardane, R.N., Martin, O.C., Cao, K., Zhang, L.J., Dej, K., Iwamatsu, A., and Zheng, Y.X. (2000). Characterization and reconstitution of Drosophila g-tubulin ring complex subunits. J. Cell Biol. 151: 1513-1523.
19. Guo, L., Ho, C.-M.K., Kong, Z., Lee, Y.-R.J., Qian, Q., and Liu, B. (2009). Evaluating the microtubule cytoskeleton and its interacting proteins in monocots by mining the rice genome. Ann. Bot. (Lond.) 103: 387-402.
20. Hallen, M.A., Ho, J., Yankel, C.D., and Endow, S.A. (2008). Fluorescence recovery kinetic analysis of g-tubulin binding to the mitotic spindle. Biophys. J. 95: 3048-3058.
21. Hamada, T. (2007). Microtubule-associated proteins in higher plants. J. Plant Res. 120: 79-98.
22. Horio, T., Basaki, A., Takeoka, A., and Yamato, M. (1999). Lethal level overexpression of g-tubulin in fission yeast causes mitotic arrest. Cell Motil. Cytoskeleton 44: 284-295.
23. Ishida, T., Kurata, T., Okada, K., and Wada, T. (2008). A genetic regulatory network in the development of trichomes and root hairs. Annu. Rev. Plant Biol. 59: 365-386.
24. Izumi, N., Fumoto, K., Izumi, S., and Kikuchi, A. (2008). GSK-3b regulates proper mitotic spindle formation in cooperation with a component of the g-tubulin ring complex, GCP5. J. Biol. Chem. 283: 12981-12991.
25. Jeng, R., and Stearns, T. (1999). g-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. Julian, M., Tollon, Y., Lajoie-Mazenc, I., Moisand, A., Mazarguil, H., Puget, A., and Wright, A. (1993). g-Tubulin participates in the formation of the midbody during cytokinesis in mammalian cells. J. Cell Sci. 105: 145-156.
28. Kong, Z., Li, M., Yang, W., Xu, W., and Xue, Y. (2006). A novel nuclearlocalized CCCH-type zinc finger protein, OsDOS, is involved in delaying leaf senescence in rice. Plant Physiol. 141: 1376-1388.
29. Lajoie-Mazenc, I., Tollon, Y., Detraves, C., Julian, M., Moisand, A., Gueth-Hallonet, C., Debec, A., Salles-Passador, I., Puget, A., Mazarguil, H., Raynaud-Messina, B., and Wright, M. (1994). Recruitment of antigenic g-tubulin during mitosis in animal cells: presence of g-tubulin in the mitotic spindle. J. Cell Sci. 107: 2825-2837.
30. Lee, Y.-R.J., Giang, H.M., and Liu, B. (2001). A novel plant kinesinrelated protein specifically associates with the phragmoplast organelles. Plant Cell 13: 2427-2439.
31. Lee, Y.R.J., and Liu, B.(2000).Identificationofaphragmoplast-associated kinesin-related protein in higher plants. Curr. Biol. 10: 797-800.
32. Liu, B., Joshi, H.C., and Palevitz, B.A. (1995). Experimental manipulation of g-tubulin distribution in Arabidopsis using antimicrotubule drugs. Cell Motil. Cytoskeleton 31: 113-129.
33. Liu, B., Joshi, H.C., Wilson, T.J., Silflow, C.D., Palevitz, B.A., and Snustad, D.P. (1994). g-Tubulin in Arabidopsisgene sequence, immunoblot, and immunofluorescence studies. Plant Cell 6: 303-314.
34. Liu, B., Marc, J., Joshi, H.C., and Palevitz, B.A. (1993). A g-tubulinrelated protein associated with the microtubule arrays of higher plants in a cell cycle-dependent manner. J. Cell Sci. 104: 1217-1228.
35. Lu, L., Lee, Y.-R.J., Pan, R., and Liu, B. (2005). An internal motor kinesin is associated with the Golgi apparatus and plays a role in trichome morphogenesis in Arabidopsis. Mol. Biol. Cell 16: 811-823.
36. Lüders, J., and Stearns, T. (2007). Microtubule-organizing centres: A re-evaluation. Nat. Rev. Mol. Cell Biol. 8: 161-167.
37. Marc, J., Mineyuki, Y., and Palevitz, B.A. (1989). A planar microtubule- organizing zone in guard-cells of Allium - Experimental depolymerization and reassembly of microtubules. Planta 179: 530-540.
38. McDonald, A.R., Liu, B., Joshi, H.C., and Palevitz, B.A. (1993). g-Tubulin is associated with a cortical-microtubule-organizing zone in the developing guard cells of Allium cepa L. Planta 191: 357-361.
39. 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 g-tubulin in higher plants. Nat. Cell Biol. 7: 961-968.
40. Murata, T., Tanahashi, T., Nishiyama, T., Yamaguchi, K., and Hasebe, M. (2007). How do plants organize microtubules without a centrosome? J. Integr. Plant Biol. 49: 1154-1163.
41. Murphy, S.M., Preble, A.M., Patel, U.K., O'Connell, K.L., Dias, D.P., Moritz, M., Agard, D., Stults, J.T., and Stearns, T. (2001). GCP5 and GCP6: Two new members of the human g-tubulin complex. Mol. Biol. Cell 12: 3340-3352.
42. Murphy, S.M., Urbani, L., and Stearns, T. (1998). The mammalian g-tubulin complex contains homologues of the yeast spindle pole body components spc97p and spc98p. J. Cell Biol. 141: 663-674.
43. 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.
44. Nakamura, M., and Hashimoto, T. (2009). A mutation in the Arabidopsis g-tubulin-containing complex causes helical growth and abnormal microtubule branching. J. Cell Sci. 122: 2208-2217.
45. 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.
46. Olmsted, J.B. (1981). Affinity purification of antibodies from diazotized paper blots of heterogeneous protein samples. J. Biol. Chem. 256: 11955-11957.
47. Paluh, J.L., Nogales, E., Oakley, B.R., McDonald, K., Pidoux, A.L., and Cande, W.Z. (2000). A mutation in g-tubulin alters microtubule dynamics and organization and is synthetically lethal with the kinesin-like protein pkl1p. Mol. Biol. Cell 11: 1225-1239.
48. Pastuglia, M., Azimzadeh, J., Goussot, M., Camilleri, C., Belcram, K., Evrard, J.L., Schmit, A.C., Guerche, P., and Bouchez, D. (2006). g-Tubulin is essential for microtubule organization and development in Arabidopsis. Plant Cell 18: 1412-1425.
49. Raynaud-Messina, B., and Merdes, A. (2007). g-Tubulin complexes and microtubule organization. Curr. Opin. Cell Biol. 19: 24-30.
50. Samejima, I., Lourenco, P.C.C., Snaith, H.A., and Sawin, K.E. (2005). Fission yeast mto2p regulates microtubule nucleation by the centrosomin-related protein mto1p. Mol. Biol. Cell 16: 3040-3051.
51. Sawin, K.E., and Tran, P.T. (2006). Cytoplasmic microtubule organization in fission yeast. Yeast 23: 1001-1014.
52. Schwab, R., Ossowski, S., Riester, M., Warthmann, N., and Weigel, D. (2006). Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18: 1121-1133.
53. Seltzer, V., Janski, N., Canaday, J., Herzog, E., Erhardt, M., Evrard, J.L., and Schmit, A.C. (2007). Arabidopsis GCP2 and GCP3 are part of a soluble gamma-tubulin complex and have nuclear envelope targeting domains. Plant J. 52: 322-331.
54. Shimamura, M., Brown, R.C., Lemmon, B.E., Akashi, T., Mizuno, K., Nishihara, N., Tomizawa, K., Yoshimoto, K., Deguchi, H., Hosoya, H., Horio, T., and Mineyuki, Y. (2004). g-Tubulin in basal land plants: Characterization, localization, and implication in the evolution of acentriolar microtubule organizing centers. Plant Cell 16: 45-59.
55. Silflow, C.D., Liu, B., LaVoie, M., Richardson, E.A., and Palevitz, B.A. (1999). g-Tubulin in Chlamydomonas: Characterization of the gene and localization of the gene product in cells. Cell Motil. Cytoskeleton 42: 285-297.
56. Stoppin-Mellet, V., Peter, C., and Lambert, A.M. (2000). Distribution of g-tubulin in higher plant cells: Cytosolic g-tubulin is part of higher molecular weight complexes. Plant Biol. 2: 290-296.
57. Venkatram, S., Tasto, J.J., Feoktistova, A., Jennings, J.L., Link, A.J., and Gould, K.L. (2004). Identification and characterization of two novel proteins affecting fission yeast g-tubulin complex function. Mol. Biol. Cell 15: 2287-2301.
58. Vérollet, C., Colombié, N., Daubon, T., Bourbon, H.M., Wright, M., and Raynaud-Messina, B. (2006). Drosophila melanogaster g-TuRC is dispensable for targeting g-tubulin to the centrosome and microtubule nucleation. J. Cell Biol. 172: 517-528.
59. Vinh, D.B., Kern, J.W., Hancock, W.O., Howard, J., and Davis, T.N. (2002). Reconstitution and characterization of budding yeast g-tubulin complex. Mol. Biol. Cell 13: 1144-1157.
60. Wasteneys, G. (2002). Microtubule organization in the green kingdom: Chaos or self-order? J. Cell Sci. 115: 1345-1354.
61. Wiese, C., and Zheng, Y. (2006). Microtubule nucleation: g-Tubulin and beyond. J. Cell Sci. 119: 4143-4153.
62. Xiong, Y., and Oakley, B.R. (2009). In vivo analysis of the functions of g-tubulin complex proteins. J. Cell Sci. 122: 4218-4227.
63. Zeng, C.J., Lee, Y.R., and Liu, B. (2009). The WD40 repeat protein NEDD1 functions in microtubule organization during cell division in Arabidopsis thaliana. Plant Cell 21: 1129-1140.
64. Zheng, Y., Wong, M.L., Alberts, B., and Mitchison, T. (1995). Nucleation of microtubule assembly by a g-tubulin-containing ring complex. Nature 378: 578-583.
65. Zimmerman, S., and Chang, F. (2005). Effects of g-tubulin complex proteins on microtubule nucleation and catastrophe in fission yeast. Mol. Biol. Cell 16: 2719-2733.