Cortical microtubule arrays undergo rotary movements in Arabidopsis hypocotyl epidermal cells

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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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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.

Author information

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.

Correspondence to Jordi Chan.

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The authors declare no competing financial interests.

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