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Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments

Nature Cell Biology volume 11, pages 797–806 (2009)Cite this article

Abstract

Plant cell morphogenesis relies on the organization and function of two polymer arrays separated by the plasma membrane: the cortical microtubule cytoskeleton and cellulose microfibrils in the cell wall. Studies using in vivo markers confirmed that one function of the cortical microtubule array is to drive organization of cellulose microfibrils by guiding the trajectories of active cellulose synthase (CESA) complexes in the plasma membrane, thus orienting nascent microfibrils. Here we provide evidence that cortical microtubules also position the delivery of CESA complexes to the plasma membrane and interact with small CESA-containing compartments by a mechanism that permits motility driven by microtubule depolymerization. The association of CESA compartments with cortical microtubules was greatly enhanced during osmotic stress and other treatments that limit cellulose synthesis. On recovery from osmotic stress, delivery of CESA complexes to the plasma membrane was observed in association with microtubule-tethered compartments. These results reveal multiple functions for the microtubule cortical array in organizing CESA in the cell cortex.

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Figure 1: Delivery of CESA complexes to the plasma membrane is coincident with microtubules.
Figure 2: CESA complex delivery is correlated with cortical Golgi body distribution.
Figure 3: Isoxaben, osmotic stress and brefeldin A redistribute CESA protein and alter the location and dynamics of compartments containing CESA.
Figure 4: SmaCCs associate with cortical microtubules in cells treated with isoxaben.
Figure 5: CESA tracks depolymerizing microtubule ends.
Figure 6: SmaCCs are associated with CESA complex delivery to the plasma membrane.
Figure 7: Successive break-up of one SmaCC into multiple cytoplasmic compartments.
Figure 8: SYP41 and SYP61 label a subset of SmaCCs.

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Acknowledgements

We thank S. Vernhettes, E. Nielsen and N. Geldner for providing transgenic Arabidopsis seeds; V. Kirik for help with vector construction; B. Busse for modifying the ImageJ frame alignment plugin; and S. Debolt, V. Kirik, R. Brown, T. Ketelaar and H. Höfte for helpful discussions. This work was supported by grants from the National Science Foundation (0524334) and the EU Commission (FP6-2004-NEST-C1-028974).

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Authors and Affiliations

  1. Department of Plant Biology, Carnegie Institution for Science, 260 Panama St, Stanford, 94305, CA, USA

    Ryan Gutierrez & David W. Ehrhardt

  2. Department of Biology, Stanford University, Stanford, 94305, CA, USA

    Ryan Gutierrez & David W. Ehrhardt

  3. Laboratory of Plant Cell Biology, Wageningen University, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands

    Jelmer J. Lindeboom & Anne Mie C. Emons

  4. Department of Molecular and Cellular Biology, University of California, Berkeley, 94720, CA, USA

    Alex R. Paredez

  5. Department of Biomolecular Systems, FOM Institute for Atomic and Molecular Physics, Kruislaan 407, 1098 SJ Amsterdam, The Netherlands

    Anne Mie C. Emons

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Contributions

R.G., J.L. and D.E. designed, carried out and analysed experiments; A.P. created the pCESA6::CFP::CESA6 and 35S::YFP::TUA5 transgenic lines; R.G. made all figures and movies; R.G., D.E. and A.M.E. wrote the manuscript.

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Correspondence to David W. Ehrhardt.

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Gutierrez, R., Lindeboom, J., Paredez, A. et al. Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments. Nat Cell Biol 11, 797–806 (2009). https://doi.org/10.1038/ncb1886

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