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Cortical microtubule arrays undergo rotary movements in Arabidopsis hypocotyl epidermal cells

Nature Cell Biology volume 9, pages 171–175 (2007)Cite this article

Abstract

Plant-cell expansion is controlled by cellulose microfibrils in the wall1 with microtubules providing tracks for cellulose synthesizing enzymes2. Microtubules can be reoriented experimentally3,4,5,6,7,8,9,10,11 and are hypothesized to reorient cyclically in aerial organs12,13,14, but the mechanism is unclear. Here, Arabidopsis hypocotyl microtubules wershee labelled with AtEB1a–GFP (Arabidopsis microtubule end-binding protein 1a) or GFP–TUA6 (Arabidopsis α-tubulin 6) to record long cycles of reorientation. This revealed microtubules undergoing previously unseen clockwise or counter-clockwise rotations. Existing models emphasize selective shrinkage and regrowth15 or the outcome of individual microtubule encounters to explain realignment16. Our higher-order view emphasizes microtubule group behaviour over time. Successive microtubules move in the same direction along self-sustaining tracks. Significantly, the tracks themselves migrate, always in the direction of the individual fast-growing ends, but twentyfold slower. Spontaneous sorting of tracks into groups with common polarities generates a mosaic of domains. Domains slowly migrate around the cell in skewed paths, generating rotations whose progressive nature is interrupted when one domain is displaced by collision with another. Rotary movements could explain how the angle of cellulose microfibrils can change from layer to layer in the polylamellate cell wall.

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Figure 1: Arabidopsis hypocotyl epidermal cells expressing AtEB1a–GFP display rotary microtubule reorientations.
Figure 2: Microtubules moving as a mosaic of polarized domains.
Figure 3: Reconstruction of polarized domains.
Figure 4: The long-term migratory pattern of AtEB1a–GFP comets over the outer cell surface.

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References

  1. Giddings, T. H. & Staehelin, A. Microtubule-mediated control of microfibril deposition: A re-examination of the hypothesis (ed. Lloyd, C. W.) (Academic Press Ltd., London, 1991).

    Google Scholar 

  2. Paredez, A. R., Somerville, C. R. & Ehrhardt, D. W. Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312, 1491–1495 (2006).

    Article  CAS  Google Scholar 

  3. Iwata, T. & Hogetsu, T. The effect of light irradiation on the orientation of microtubules in seedlings of Avena sativa L. Plant Cell Physiol. 30, 1011–1016 (1989).

    CAS  Google Scholar 

  4. Nick, P., Bergfeld, R., Schafer, E. & Schopfer, P. Unilateral reorientation of microtubules at the outer epidermal wall during photo- and gravitropic curvature of maize coleoptiles and sunflower hypocotyls. Planta 181, 162–168 (1990).

    Article  CAS  Google Scholar 

  5. Laskowski, M. Microtubule orientation in pea stem cells: a change in orientation follows the initiation of growth rate decline. Planta 181, 44–52 (1990).

    Article  CAS  Google Scholar 

  6. Ishida, K. & Katsumi, M. Immunofluorescence microscopical observation of cortical microtubule arrangement as affected by gibberellin d5 mutant of Zea mays L. Plant Cell Physiol. 32, 409–417 (1991).

    Article  CAS  Google Scholar 

  7. Ishida, K. & Katsumi, M. Effects of gibberelin and abscisic acid on the cortical microtubule orientation in hypocotyls of light-grown cucumber seedlings. Int. J. Plant Sci. 153, 155–163 (1992).

    Article  CAS  Google Scholar 

  8. Zandomeni, K. & Schopfer, P. Reorientation of microtubules at the outer epidermal wall of maize coleoptiles by phytochrome, by blue-light photoreceptor and auxin. Protoplasma 173, 103–112 (1993).

    Article  Google Scholar 

  9. Yuan, M., Shaw, P. J., Warn, R. M. & Lloyd, C. W. Dynamic reorientation of cortical microtubules, from transverse to longitudinal, in living plant cells. Proc. Natl Acad. Sci. USA 91, 6050–6053 (1994).

    Article  CAS  Google Scholar 

  10. Lloyd, C. W., Shaw, P. J., Warn, R. M. & Yuan, M. Gibberellic acid-induced reorientation of cortical microtubules in living plant cells. J. Micros. 181, 140–144 (1996).

    Article  Google Scholar 

  11. Ueda, K. & Matsuyama, T. Rearrangement of cortical microtubules from transverse to oblique or longitudinal in living cells of transgenic Arabidopsis thaliana. Protoplasma 213, 28–38 (2000).

    Article  CAS  Google Scholar 

  12. Mayumi, K. & Shibaoka, H. The cyclic reorientation of cortical microtubules on walls with a crossed polylamellate structure: effects of plant hormones and an inhibitor of protein kinases on the progression of the cycle. Protoplasma 195, 112–122 (1996).

    Article  CAS  Google Scholar 

  13. Takesue, K. & Shibaoka, H. The cyclic reorientation of cortical microtubules in epidermal cells of azuki bean epicotyls: the role of actin filaments in the progression of the cycle. Planta 205, 539–546 (1998).

    Article  CAS  Google Scholar 

  14. Hejnowicz, Z. Autonomous changes in the orientation of cortical microtubules underlying the helicoidal cell wall of the sunflower hypocotyl epidermis: spatial variation translated into temporal changes. Protoplasma 225, 243–256 (2005).

    Article  CAS  Google Scholar 

  15. Yuan, M., Warn, R. M., Shaw, P. J. & Lloyd, C. W. Dynamic microtubules under the radial and outer tangential walls of microinjected pea epidermal cells observed by computer reconstruction. Plant J. 7, 17–23 (1995).

    Article  CAS  Google Scholar 

  16. Dixit, R. & Cyr, R. Encounters between dynamic cortical microtubules promote ordering of the cortical array through angle-dependent modifications of microtubule behavior. Plant Cell 16, 3274–3284 (2004).

    Article  CAS  Google Scholar 

  17. Sugimoto, K., Willamson, R. E. & Wasteneys, G. O. New techniques enable comparative analysis of microtubule orientation, wall texture, and growth rate in intact roots of Arabidopsis. Plant Physiol. 124, 1493–1506 (2000).

    Article  CAS  Google Scholar 

  18. Buschmann, H. et al. Helical growth of the Arabidopsis mutant tortifolia1 reveals a plant-specific microtubule-associated protein. Curr. Biol. 14, 1515–1521 (2004).

    Article  CAS  Google Scholar 

  19. Le, J., Vandenbussche, F., De Cnodder, T., Van Der Straeten, D. & Verbelen, J.-P. Cell elongation and microtubule behavior in the Arabidopsis hypocotyl: responses to ethylene and auxin. J. Plant Growth Regul. 24, 166–178 (2005).

    Article  CAS  Google Scholar 

  20. Nakajima, K., Kawamura, T. & Hashimoto Role of the SPIRAL1 gene family in anisotropic growth of Arabidopsis thaliana. Plant Cell Physiol. 47, 513–522 (2006).

    Article  CAS  Google Scholar 

  21. Hush, J. M., Wadsworth, P., Callaham, D. A. & Hepler, P. K. Quantification of microtubule dynamics in living plant cells using fluorescence redistribution after photobleaching. J. Cell Sci. 107, 775–784 (1994).

    PubMed  Google Scholar 

  22. Shaw, S. L., Kamyar, R. & Ehrhardt, D. W. Sustained microtubule treadmilling in Arabidopsis cortical arrays. Science 300, 1715–1718 (2003).

    Article  CAS  Google Scholar 

  23. Chan, J., Calder, G., Fox, S. & Lloyd, C. Localization of the end-bidning protein EB1 reveals alternative pathways of spindle development in Arabidopsis suspension cells. Plant Cell 17, 1737–1748 (2005).

    Article  CAS  Google Scholar 

  24. Chan, J., Calder, G. M., Doonan, J. H. & Lloyd, C. W. EB1 reveals mobile microtubule nucleation sites in Arabidopsis. Nature Cell Biol. 5, 967–971 (2003).

    Article  CAS  Google Scholar 

  25. Dhonukshe, P., Mathur, J., Hulskamp, M. & Gadella, T. W., Jr. Microtubule plus-ends reveal essential links between intracellular polarization and localized modulation of endocytosis during division-plane establishment in plant cells. BMC Biol 3, 11 (2005).

    Article  Google Scholar 

  26. Dixit, R., Chang, E. & Cyr, R. Establishment of polarity during organization of the acentrosomal plant cortical microtubule array. Mol. Biol. Cell. 17, 1298–1305 (2006).

    Article  CAS  Google Scholar 

  27. Gendreau, E. et al. Cellular basis of hypocotyl growth in Arabidopsis thaliana. Plant Physiol. 114, 295–305 (1997).

    Article  CAS  Google Scholar 

  28. Refrégier, G., Pelletire, S., Jaillard, D. & Höfte, H. Interaction between wall deposition and cell elongation in dark-grown hypocotyl cells in Arabidopsis. Plant Physiol. 135, 1–10 (2004).

    Article  Google Scholar 

  29. Ueda, K., Matsuyama, T. & Hashimoto, T. Visualization of microtubules in living cells of transgenic Arabidopsis thaliana. Protoplasma 206, 201–206 (1999).

    Article  Google Scholar 

  30. Penfold, R., Watson, A. D., Mackie, A. R. & Hibberd, D. J. Quantitative imaging of aggregated emulsions. Langmuir 22, 2005–2015 (2006).

    Article  CAS  Google Scholar 

  31. Costa, M. M., Fox, S., Hanna, A. I., Baxter, C. & Coen, E. Evolution of regulatory interactions controlling floral asymmetry. Development 132, 5093–5101 (2005).

    Article  CAS  Google Scholar 

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Acknowledgements

We are grateful to E. Coen for useful discussions, H. Jones for technical support, J. Rothe for assistance with time-lapse montages and A. Mackie for assistance with vertical imaging. The work was funded by a grant-in-aid to the John Innes Centre by the Biotechnology and Biological Sciences Research Council.

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  1. Department of Cell and Developmental Biology, John Innes Centre, Norwich, NR4 7UH, UK

    Jordi Chan, Grant Calder, Samantha Fox & Clive Lloyd

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  1. Jordi Chan
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  3. Samantha Fox
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Contributions

J.C. contributed to project planning, collection of experimental data, data analysis, supervision and writing. G.C. contributed to the collection of experimental data and data analysis. S.F. produced the AtEB1–GFP lines. C.L. was responsible for supervision and writing.

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Correspondence to Jordi Chan.

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The authors declare no competing financial interests.

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Chan, J., Calder, G., Fox, S. et al. Cortical microtubule arrays undergo rotary movements in Arabidopsis hypocotyl epidermal cells. Nat Cell Biol 9, 171–175 (2007). https://doi.org/10.1038/ncb1533

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