This Article Full Text Full Text (PDF) Supplemental Data All Versions of this Article: 16/12/3274    most recent tpc.104.026930v1 Alert me when this article is cited Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via ISI Web of Science (39) Citing Articles via Google Scholar Google Scholar Articles by Dixit, R. Articles by Cyr, R. Search for Related Content PubMed PubMed Citation Articles by Dixit, R. Articles by Cyr, R. Agricola Articles by Dixit, R. Articles by Cyr, R.

Encounters between Dynamic Cortical Microtubules Promote Ordering of the Cortical Array through Angle-Dependent Modifications of Microtubule Behavior

Penn State University, University Park, Pennsylvania 16802

¹ To whom correspondence should be addressed. E-mail rvd10{at}psu.edu; fax 814-865-9131.

Ordered cortical microtubule arrays are essential for normal plant morphogenesis, but how these arrays form is unclear. The dynamics of individual cortical microtubules are stochastic and cannot fully account for the observed order; however, using tobacco (Nicotiana tabacum) cells expressing either the MBD-DsRed (microtubule binding domain of the mammalian MAP4 fused to the Discosoma sp red fluorescent protein) or YFP-TUA6 (yellow fluorescent protein fused to the Arabidopsis -tubulin 6 isoform) microtubule markers, we identified intermicrotubule interactions that modify their stochastic behaviors. The intermicrotubule interactions occur when the growing plus-ends of cortical microtubules encounter previously existing cortical microtubules. Importantly, the outcome of such encounters depends on the angle at which they occur: steep-angle collisions are characterized by approximately sevenfold shorter microtubule contact times compared with shallow-angle encounters, and steep-angle collisions are twice as likely to result in microtubule depolymerization. Hence, steep-angle collisions promote microtubule destabilization, whereas shallow-angle encounters promote both microtubule stabilization and coalignment. Monte Carlo modeling of the behavior of simulated microtubules, according to the observed behavior of transverse and longitudinally oriented cortical microtubules in cells, reveals that these simple rules for intermicrotubule interactions are necessary and sufficient to facilitate the self-organization of dynamic microtubules into a parallel configuration.

This article has been cited by other articles:

				A. R. Paredez, S. Persson, D. W. Ehrhardt, and C. R. Somerville Genetic Evidence That Cellulose Synthase Activity Influences Microtubule Cortical Array Organization Plant Physiology, August 1, 2008; 147(4): 1723 - 1734. [Abstract] [Full Text] [PDF]

				M. Yao, Y. Wakamatsu, T. J. Itoh, T. Shoji, and T. Hashimoto Arabidopsis SPIRAL2 promotes uninterrupted microtubule growth by suppressing the pause state of microtubule dynamics J. Cell Sci., July 15, 2008; 121(14): 2372 - 2381. [Abstract] [Full Text] [PDF]

				D. A. Barton, M. Vantard, and R. L. Overall 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, April 1, 2008; 20(4): 982 - 994. [Abstract] [Full Text] [PDF]

				N. A. Eckardt High-Resolution Imaging of Cortical Microtubule Arrays PLANT CELL, April 1, 2008; 20(4): 817 - 819. [Full Text] [PDF]

				J. C. Ambrose, T. Shoji, A. M. Kotzer, J. A. Pighin, and G. O. Wasteneys The Arabidopsis CLASP Gene Encodes a Microtubule-Associated Protein Involved in Cell Expansion and Division PLANT CELL, September 1, 2007; 19(9): 2763 - 2775. [Abstract] [Full Text] [PDF]

				A. V. Korolev, H. Buschmann, J. H. Doonan, and C. W. Lloyd AtMAP70-5, a divergent member of the MAP70 family of microtubule-associated proteins, is required for anisotropic cell growth in Arabidopsis J. Cell Sci., July 1, 2007; 120(13): 2241 - 2247. [Abstract] [Full Text] [PDF]

				T. Ishida, Y. Kaneko, M. Iwano, and T. Hashimoto Helical microtubule arrays in a collection of twisting tubulin mutants of Arabidopsis thaliana PNAS, May 15, 2007; 104(20): 8544 - 8549. [Abstract] [Full Text] [PDF]

				M. C. Lagomarsino, C. Tanase, J. W. Vos, A. M. C. Emons, B. M. Mulder, and M. Dogterom Microtubule Organization in Three-Dimensional Confined Geometries: Evaluating the Role of Elasticity Through a Combined In Vitro and Modeling Approach Biophys. J., February 1, 2007; 92(3): 1046 - 1057. [Abstract] [Full Text] [PDF]

				J. C. Ambrose and R. Cyr The Kinesin ATK5 Functions in Early Spindle Assembly in Arabidopsis PLANT CELL, January 1, 2007; 19(1): 226 - 236. [Abstract] [Full Text] [PDF]

				P. Dhonukshe, N. Vischer, and T. W. J. Gadella Jr Contribution of microtubule growth polarity and flux to spindle assembly and functioning in plant cells. J. Cell Sci., August 1, 2006; 119(Pt 15): 3193 - 3205. [Abstract] [Full Text] [PDF]

				N. A. Eckardt Function of {gamma}-Tubulin in Plants PLANT CELL, June 1, 2006; 18(6): 1327 - 1329. [Full Text] [PDF]

				P. Binarova, V. Cenklova, J. Prochazkova, A. Doskocilova, J. Volc, M. Vrlik, and L. Bogre {gamma}-Tubulin Is Essential for Acentrosomal Microtubule Nucleation and Coordination of Late Mitotic Events in Arabidopsis PLANT CELL, May 1, 2006; 18(5): 1199 - 1212. [Abstract] [Full Text] [PDF]

				R. Dixit, E. Chang, and R. Cyr Establishment of Polarity during Organization of the Acentrosomal Plant Cortical Microtubule Array Mol. Biol. Cell, March 1, 2006; 17(3): 1298 - 1305. [Abstract] [Full Text] [PDF]

				A. Reilein, S. Yamada, and W. J. Nelson Self-organization of an acentrosomal microtubule network at the basal cortex of polarized epithelial cells J. Cell Biol., December 5, 2005; 171(5): 845 - 855. [Abstract] [Full Text] [PDF]