A three-dimensional computer simulation model reveals the mechanisms for self-organization of plant cortical microtubules into oblique arrays

Molecular Biology of the Cell

Volumn 21, Issue 15, 2010, Pages 2674-2684

  Eren, Ezgi Can ^a   Dixit, Ram ^b   Gautam, Natarajan ^a  

^a Texas AandM University   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARTICLE; COMPUTER SIMULATION; MICROTUBULE; PLANT CELL; PLANT GENE; PLANT GROWTH; PRIORITY JOURNAL; THREE DIMENSIONAL IMAGING;

ARABIDOPSIS; CELL POLARITY; COMPUTER SIMULATION; MICROTUBULES; MODELS, MOLECULAR; MUTATION; PHENOTYPE;

ARABIDOPSIS;

EID: 77955118991     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E10-02-0136     Document Type: Article

References (49)

1. Abe, T., Thitamadee, S., and Hashimoto, T. (2004). Microtubule defects and cell morphogenesis in the lefty1lefty2 tubulin mutant of Arabidopsis thaliana. Plant Cell Physiol. 45, 211-220.
2. Allard, J. F., Wasteneys, G. O., and Cytrynbaum, E. N. (2010). Mechanisms of self-organization of cortical microtubules in plants revealed by computational simulations. Mol. Biol. Cell 21, 278-286.
3. Ambrose, J. C., and Wasteneys, G. O. (2008). CLASP modulates microtubule-cortex interaction during self-organization of acentrosomal microtubules. Mol. Biol. Cell 19, 4730-4737.
4. Balch, T. (2000). Hierarchic social entropy: an information theoretic measure of robot group diversity. Autonomous Robots 8, 209-237.
5. Barton, D. A., Vantard, M., and Overall, R. L. (2008). Analysis of cortical arrays from Tradescantia virginiana at high resolution reveals discrete microtubule subpopulations and demonstrates that confocal images of arrays can be misleading. Plant Cell 20, 982-994.
6. Baulin, V. A., Marques, C. M., and Thalmann, F. (2007). Collision induced spatial organization of microtubules. Biophys. Chem. 128, 231-244.
7. 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.
8. Burk, D. H., Liu, B., Zhong, R., 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.
9. 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.
10. Buschmann, H., Fabri, C. O., Hauptmann, M., Hutzler, P., Laux, T., Lloyd, C. W., and Schaffner, A. R. (2004). Helical growth of the Arabidopsis mutant tortifolia1 reveals a plant-specific microtubule-associated protein. Curr. Biol. 14, 1515-1521.
11. Buschmann, H., Hauptmann, M., Niessing, D., Lloyd, C. W., and Schaffner, A. R. (2009). Helical growth of the Arabidopsis mutant tortifolia2 does not depend on cell division patterns but involves handed twisting of isolated cells. Plant Cell 21, 2090-2106.
12. Bustos, M. M., Guiltinan, M. J., Cyr, R. J., Ahdoot, D., and Fosket, D. E. (1989). Light Regulation of beta-tubulin gene expression during internode development in soybean (Glycine max [L.] Merr.). Plant Physiol. 91, 1157-1161.
13. 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.
14. 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.
15. Dixit, R., Chang, E., and Cyr, R. (2006). Establishment of polarity during organization of the acentrosomal plant cortical microtubule array. Mol. Biol. Cell 17, 1298-1305.
16. Dixit, R., and Cyr, R. (2004a). The cortical microtubule array: from dynamics to organization. Plant Cell 16, 2546-2552.
17. Dixit, R., and Cyr, R. (2004b). Encounters between dynamic cortical microtubules promote ordering of the cortical array through angle-dependent modifications of microtubule behavior. Plant Cell 16, 3274-3284.
18. Ehrhardt, D. W., and Shaw, S. L. (2006). Microtubule dynamics and organization in the plant cortical array. Annu. Rev. Plant Biol. 57, 859-875.
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. Granger, C. L., and Cyr, R. J. (2001). Spatiotemporal relationships between growth and microtubule orientation as revealed in living root cells of Arabidopsis thaliana transformed with green-fluorescent-protein gene construct GFP-MBD. Protoplasma 216, 201-214.
21. Gray, R. M. (1990). Entropy and Information Theory, Springer-Verlag: New York.
22. Hardham, A. R., and Gunning, B. E. (1978). Structure of cortical microtubule arrays in plant cells. J. Cell Biol. 77, 14-34.
23. Ishida, T., Kaneko, Y., Iwano, M., and Hashimoto, T. (2007a). Helical microtubule arrays in a collection of twisting tubulin mutants of Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 104, 8544-8549.
24. Ishida, T., Thitamadee, S., and Hashimoto, T. (2007b). Twisted growth and organization of cortical microtubules. J. Plant Res. 120, 61-70. (Pubitemid 46317762)
25. Kawamura, E., and Wasteneys, G. O. (2008). MOR1, the Arabidopsis thaliana homologue of Xenopus MAP215, promotes rapid growth and shrinkage, and suppresses the pausing of microtubules in vivo. J. Cell Sci. 121, 4114-4123.
26. Kerssemakers, J. W., Munteanu, E. L., Laan, L., Noetzel, T. L., Janson, M. E., and Dogterom, M. (2006). Assembly dynamics of microtubules at molecular resolution. Nature 442, 709-712.
27. Kong, Z., Hotta, T., Lee, Y.R., Horio, T., and Liu, B. (2010). The γ-tubulin complex protein GCP4 is required for organizing functional microtubule arrays in Arabidopsis thaliana. Plant Cell 22, 191-204.
28. Lu, J. L., Valois, F., Dohler, M., and Barthel, D. (2008). Quantifying organization by means of entropy. IEEE Commun. Lett. 12, 185-187.
29. Marc, J., Granger, C. L., Brincat, J., Fisher, D. D., Kao, T., 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, 1927-1940.
30. Martin, M. T., Plastinoa, A., and Rossob, O. A. (2006). Generalized statistical complexity measures: geometrical and analytical properties. Physica A 369, 439-462.
31. 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.
32. Nakajima, K., Furutani, I., Tachimoto, H., Matsubara, H., 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.
33. Nakajima, K., Kawamura, T., and Hashimoto, T. (2006). Role of the SPIRAL1 gene family in anisotropic growth of Arabidopsis thaliana. Plant Cell Physiol. 47, 513-522.
34. Nakamura, M., and Hashimoto, T. (2009). A mutation in the Arabidopsis gamma-tubulin-containing complex causes helical growth and abnormal microtubule branching. J. Cell Sci. 122, 2208-2217.
35. Shannon, C. E. (1948). A mathematical theory of communication. Bell System Tech. J. 27, 379-423.
36. Shaw, S. L., Kamyar, R., and Ehrhardt, D. W. (2003). Sustained microtubule treadmilling in Arabidopsis cortical arrays. Science 300, 1715-1718.
37. Sugimoto, K., Himmelspach, R., Williamson, R. E., and Wasteneys, G. O. (2003). Mutation or drug-dependent microtubule disruption causes radial swelling without altering parallel cellulose microfibril deposition in Arabidopsis root cells. Plant Cell 15, 1414-1429. (Pubitemid 36715182)
38. Sunohara, H., Kawai, T., Shimizu-Sato, S., Sato, Y., Sato, K., and Kitano, H. (2009). A dominant mutation of TWISTED DWARF 1 encoding an alpha-tubulin protein causes severe dwarfism and right helical growth in rice. Genes Genet. Syst. 84, 209-218.
39. Szymanski, D. B., and Cosgrove, D. J. (2009). Dynamic coordination of cytoskeletal and cell wall systems during plant cell morphogenesis. Curr. Biol. 19, R800-R811.
40. Thitamadee, S., Tuchihara, K., and Hashimoto, T. (2002). Microtubule basis for left-handed helical growth in Arabidopsis. Nature 417, 193-196. (Pubitemid 34506801)
41. Traas, J. A., Braat, P., and Derksen, J. W. (1984). Changes in microtubule arrays during the differentiation of cortical root cells of Raphanus sativus. Eur J. Cell Biol. 34, 229-238.
42. Wasteneys, G. O. (2002). Microtubule organization in the green kingdom: chaos or self-order? J. Cell Sci. 115, 1345-1354.
43. Wasteneys, G. O., and Ambrose, J. C. (2009). Spatial organization of plant cortical microtubules: close encounters of the 2D kind. Trends Cell Biol. 19, 62-71.
44. Wasteneys, G. O., and Williamson, R. E. (1989a). Reassembly of microtubules in Nitella tasmanica - assembly of cortical microtubules in branching clusters and its relevance to steady-state microtubule assembly. J. Cell Sci. 93, 705-714.
45. Wasteneys, G. O., and Williamson, R. E. (1989b). Reassembly of microtubules in Nitella tasmanica - quantitative-analysis of assembly and orientation. Eur. J. Cell Biol. 50, 76-83.
46. 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.
47. Wightman, R., and Turner, S. R. (2007). Severing at sites of microtubule crossover contributes to microtubule alignment in cortical arrays. Plant J. 52, 742-751.
48. Yao, M., Wakamatsu, Y., Itoh, T. J., Shoji, T., and Hashimoto, T. (2008). Arabidopsis SPIRAL2 promotes uninterrupted microtubule growth by suppressing the pause state of microtubule dynamics. J. Cell Sci. 121, 2372-2381.
49. Yuan, M., Shaw, P. J., Warn, R. M., and Lloyd, C. W. (1994). Dynamic reorientation of cortical microtubules, from transverse to longitudinal, in living plant cells. Proc. Natl. Acad. Sci. USA 91, 6050-6053.