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Microtubules and the shape of plants to come

Nature Reviews Molecular Cell Biology volume 5, pages 13–23 (2004)Cite this article

Key Points

  • Cortical microtubules are often, but not always, parallel to the cellulose microfibrils in the cell wall: the alignment of microfibrils helps to regulate the direction in which the cell can expand.

  • Cortical microtubules are nucleated from numerous cortical sites, which are marked by end-binding protein 1 (EB1). The microtubules might be freed by the severing protein katanin and move over the cortex by a modified form of treadmilling, in which there is preferred plus-end assembly.

  • These individual cortical microtubules become organized into characteristic parallel groups, usually transverse to the direction of cell elongation. How these microtubules are ordered in the absence of a centrosome has been an important question.

  • Organization is achieved by a self-ordering process that involves microtubule-associated proteins (MAPs) that are just starting to be described. The filamentous protein MAP65 crossbridges the microtubules into parallel groups; another filament-forming protein, MOR1, also helps regulate microtubule behaviour; a phospholipase D is thought to connect the microtubules to the plasma membrane.

  • Developmental mutants show that the self-organization of the microtubules is important for cells to elongate and plants to develop an axis. The exact relationship between microtubules and cellulose microfibrils during primary growth is still undecided; however, studies on secondary cell-wall formation indicate that intramembranous cellulose-synthesizing enzymes require cortical microtubules, apparently to guide their movement.

Abstract

Plants control the direction of cell expansion as a way of shaping growth. Since their discovery in plants 40 years ago, microtubules have been suspected of forming a template that helps to regulate the direction of growth. The detailed mechanism, however, has been elusive, especially as plants lack a microtubule-organizing centre. Developmental mutants are now beginning to show how microtubules are organized and how this affects plant morphology.

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Figure 1: Transversely wound cellulose microfibrils resist lateral cell expansion.
Figure 2: Comparing the organization of plant and animal cytoplasmic microtubules.
Figure 3: Microtubules move over the plant cell's cortex by modified treadmilling.
Figure 4: Abnormal microtubule patterns in the katanin mutant fra2.
Figure 5: Abnormal cellulose deposition in cells of the katanin mutant fra2.
Figure 6: Regular cellulose organization in the microtubule mutant mor1-1.
Figure 7: Cellulose-synthesizing enzymes colocalize with microtubule bundles during xylem formation.
Figure 8: A speculative model of proteins involved in organizing the cortical microtubule array.

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References

  1. Ledbetter, M. C. & Porter, K. R. A 'microtubule' in plant cell fine structure. J. Cell Biol. 19, 239–250 (1963).

    Article  CAS  Google Scholar 

  2. Heath, I. & Seagull, R. W. In The Cytoskeleton in Plant Growth and Development (ed. Lloyd, C. W.) 163–182 (Academic, London, 1982).

    Google Scholar 

  3. Lancelle, S. A., Callaham, D. A. & Hepler, P. K. A method for rapid freeze fixation of plant cells. Protoplasma 131, 153–165 (1986)

    Article  Google Scholar 

  4. Lloyd, C. W., Chan, J. & Hussey, P. J. in The Plant Cytoskeleton in Cell Differentiation and Development (ed. Hussey, P. J.) 3–27 (Blackwell, Oxford, 2003).

    Google Scholar 

  5. Schmit, A. C. Acentrosomal microtubule nucleation in higher plants. Int. Rev. Cytol. 220, 257–289 (2002).

    Article  CAS  Google Scholar 

  6. Stoppin, V., Vantard, M., Schmit, A. C. & Lambert, A. M. Isolated plant nuclei nucleate microtubule assembly: the nuclear surface in higher plants has centrosome-like activity. Plant Cell 6, 1099–1106 (1994).

    Article  CAS  Google Scholar 

  7. 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 

  8. Granger, C. L. & Cyr, R. J. 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 (2001).

    Article  CAS  Google Scholar 

  9. Shaw, S. L., Kamyar, R. & Ehrhardt, D. W. Sustained microtubule treadmilling in Arabidopsis cortical arrays. Science 300, 1715–1718 (2003). Evidence that cortical microtubules translocate using a modified form of treadmilling.

    Article  CAS  Google Scholar 

  10. Dhonukshe, P. & Gadella, T. W. Alteration of microtubule dynamic instability during preprophase band formation revealed by yellow fluorescent protein–CLIP170 microtubule plus-end labeling. Plant Cell 15, 597–611 (2003).

    Article  CAS  Google Scholar 

  11. Lloyd, C. Why should stationary plant cells have such dynamic microtubules? Mol. Biol. Cell 5, 1277–1280 (1994).

    Article  CAS  Google Scholar 

  12. Job, D., Valiron, O. & Oakley, B. Microtubule nucleation. Curr. Opin. Cell Biol. 15, 111–117 (2003).

    Article  CAS  Google Scholar 

  13. Panteris, E., Apostolakos, P., Graf, R. & Galatis, B. γ-tubulin colocalizes with microtubule arrays and tubulin paracrystals in dividing vegetative cells of higher plants. Protoplasma 210, 179–187 (2000).

    Article  Google Scholar 

  14. Drykova, D. et al. Plant γ-tubulin interacts with αβ-tubulin dimers and forms membrane-associated complexes. Plant Cell 15, 465–480 (2003).

    Article  CAS  Google Scholar 

  15. Erhardt, M. et al. The plant Spc98p homologue colocalizes with γ-tubulin at microtubule nucleation sites and is required for microtubule nucleation. J. Cell Sci. 115, 2423–2431 (2002).

    CAS  PubMed  Google Scholar 

  16. Chan, J., Calder, G., Doonan, J. H. & Lloyd, C. W. Mobile microtubule nucleation sites revealed in Arabidopsis by EB1. EB1 reveals mobile microtubule nucleation sites in Arabidopsis. Nature Cell Biol. 5, 967–971 (2003). This work shows that cortical microtubules are nucleated from multiple foci that are labelled with the microtubule-end-binding protein, EB1.

    Article  CAS  Google Scholar 

  17. Straube, A., Brill, M., Oakley, B. R., Horio, T. & Steinberg, G. Microtubule organization requires cell cycle-dependent nucleation at dispersed cytoplasmic sites: polar and perinuclear microtubule organizing centers in the plant pathogen Ustilago maydis. Mol. Biol. Cell 14, 642–657 (2003).

    Article  CAS  Google Scholar 

  18. Rogers, S. L., Rogers, G. C., Sharp, D. J. & Vale, R. D. Drosophila EB1 is important for proper assembly, dynamics, and positioning of the mitotic spindle. J. Cell Biol. 158, 873–884 (2002).

    Article  CAS  Google Scholar 

  19. McNally, F. J., Okawa, K., Iwamatsu, A. & Vale, R. D. Katanin, the microtubule-severing ATPase, is concentrated at centrosomes. J. Cell Sci. 109, 561–567 (1996).

    CAS  PubMed  Google Scholar 

  20. McClinton, R. S., Chandler, J. S. & Callis, J. cDNA isolation, characterization, and protein intracellular localization of a katanin-like p60 subunit from Arabidopsis thaliana. Protoplasma 216, 181–190 (2001).

    Article  CAS  Google Scholar 

  21. Stoppin-Mellet, V., Gaillard, J. & Vantard, M. Functional evidence for in vitro microtubule severing by the plant katanin homologue. Biochem. J. 365, 337–342 (2002).

    Article  CAS  Google Scholar 

  22. Burk, D. H. & Ye, Z. H. Alteration of oriented deposition of cellulose microfibrils by mutation of a katanin-like microtubule-severing protein. Plant Cell 14, 2145–2160 (2002). Mutation of the microtubule-severing protein katanin is shown to perturb microtubule organization, which results in disorganization of cellulose in the cell wall.

    Article  CAS  Google Scholar 

  23. Bouquin, T., Mattsson, O., Naested, H., Foster, R. & Mundy, J. The Arabidopsis lue1 mutant defines a katanin p60 ortholog involved in hormonal control of microtubule orientation during cell growth. J. Cell Sci. 116, 791–801 (2003).

    Article  CAS  Google Scholar 

  24. Burk, D. H., Liu, B., Zhong, R., Morrison, W. H. & Ye, Z. H. A katanin-like protein regulates normal cell wall biosynthesis and cell elongation. Plant Cell 13, 807–827 (2001).

    Article  CAS  Google Scholar 

  25. Bichet, A., Desnos, T., Turner, S., Grandjean, O. & Hofte, H. BOTERO1 is required for normal orientation of cortical microtubules and anisotropic cell expansion in Arabidopsis. Plant J. 25, 137–148 (2001).

    Article  CAS  Google Scholar 

  26. Webb, M., Jouannic, S., Foreman, J., Linstead, P. & Dolan, L. Cell specification in the Arabidopsis root epidermis requires the activity of ECTOPIC ROOT HAIR 3 — a katanin-p60 protein. Development 129, 123–131 (2002).

    CAS  PubMed  Google Scholar 

  27. Duckett, C. M. & Lloyd, C. W. Gibberellic acid-induced microtubule reorientation in dwarf peas is accompanied by rapid modification of an α-tubulin isotype. Plant J. 5, 363–372 (1994).

    Article  CAS  Google Scholar 

  28. Reddy, A. S. & Day, I. S. Kinesins in the Arabidopsis genome: a comparative analysis among eukaryotes. BMC Genomics 2, 2 <http://www.biomedcentral.com/1471-2164/2/2> (2001).

    Article  CAS  Google Scholar 

  29. Zhong, R., Burk, D. H., Morrison, W. H. & Ye, Z. H. A kinesin-like protein is essential for oriented deposition of cellulose microfibrils and cell wall strength. Plant Cell 14, 3101–3117 (2002).

    Article  CAS  Google Scholar 

  30. Preuss, M. L., Delmer, D. P. & Liu, B. The cotton kinesin-like calmodulin-binding protein associates with cortical microtubules in cotton fibers. Plant Physiol. 132, 154–160 (2003).

    Article  CAS  Google Scholar 

  31. 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 

  32. Jiang, C. -J. & Sonobe, S. Identification and preliminary characterization of a 65kDa higher-plant microtubule-associated protein. J. Cell Sci. 105, 891–901 (1993).

    CAS  Google Scholar 

  33. Chan, J., Jensen, C. G., Jensen, L. C., Bush, M. & Lloyd, C. W. The 65-kDa carrot microtubule-associated protein forms regularly arranged filamentous cross-bridges between microtubules. Proc. Natl Acad. Sci. USA 96, 14931–14936 (1999).

    Article  CAS  Google Scholar 

  34. Hussey, P. J., Hawkins, T. J., Igarashi, H., Kaloriti, D. & Smertenko, A. The plant cytoskeleton: recent advances in the study of the plant microtubule-associated proteins MAP-65, MAP-190 and the Xenopus MAP215-like protein, MOR1. Plant Mol. Biol. 50, 915–924 (2002).

    Article  CAS  Google Scholar 

  35. Chan, J. et al. Identification of a MAP65 isoform involved in directional expansion of plant cells. FEBS Lett. 534, 161–163 (2003).

    Article  CAS  Google Scholar 

  36. Yasuhara, H., Muraoka, M., Shogaki, H., Mori, H. & Sonobe, S. TMBP200, a microtubule bundling polypeptide isolated from telophase tobacco BY-2 cells is a MOR1 homologue. Plant Cell Physiol. 43, 595–603 (2002).

    Article  CAS  Google Scholar 

  37. Whittington, A. T. et al. MOR1 is essential for organizing cortical microtubules in plants. Nature 411, 610–613 (2001).

    Article  CAS  Google Scholar 

  38. Twell, D. et al. MOR1/GEM1 has an essential role in the plant-specific cytokinetic phragmoplast. Nature Cell Biol. 4, 711–714 (2002).

    Article  CAS  Google Scholar 

  39. Hussey, P. J. & Hawkins, T. J. Plant microtubule-associated proteins: the HEAT is off in temperature-sensitive mor1. Trends Plant Sci. 6, 389–392 (2001).

    Article  CAS  Google Scholar 

  40. Tournebize, R. et al. Control of microtubule dynamics by the antagonistic activities of XMAP215 and XKCM1 in Xenopus egg extracts. Nature Cell Biol. 2, 13–19 (2000).

    Article  CAS  Google Scholar 

  41. Shirasu-Hiza, M., Coughlin, P. & Mitchison, T. Identification of XMAP215 as a microtubule-destabilizing factor in Xenopus egg extract by biochemical purification. J. Cell Biol. 161, 349–358 (2003).

    Article  CAS  Google Scholar 

  42. van Breugel, M., Drechsel, D. & Hyman, A. Stu2p, the budding yeast member of the conserved Dis1/XMAP215 family of microtubule-associated proteins is a plus end-binding microtubule destabilizer. J. Cell Biol. 161, 359–369 (2003).

    Article  CAS  Google Scholar 

  43. McNally, F. Microtubule dynamics: new surprises from an old MAP. Curr. Biol. 13, R597–R599 (2003).

    Article  CAS  Google Scholar 

  44. Marc, J., Sharkey, D. E., Durso, N. A., Zhang, M. & Cyr, R. J. Isolation of a 90-kD microtubule-associated protein from Tobacco membranes. Plant Cell. 8, 2127–2138 (1996).

    Article  CAS  Google Scholar 

  45. Gardiner, J. C. et al. A 90-kD phospholipase D from tobacco binds to microtubules and the plasma membrane. Plant Cell 13, 2143–2158 (2001).

    Article  CAS  Google Scholar 

  46. Gardiner, J., Collings. D. A., Harper, J. D. & Marc, J. The effects of the phospholipase D-antagonist 1-butanol on seedling development and microtubule organisation in Arabidopsis. Plant Cell Physiol. 44,687–696 (2003).

    Article  CAS  Google Scholar 

  47. Dhonukshe, P., Laxalt, A. M., Goedhart, J., Gadella, T. W. & Munnik, T. Phospholipase D activation correlates with microtubule reorganization in living plant cells. Plant Cell. 15, 2666–2679 (2003). References 44–47 show that a phospholipase D links cortical microtubules to the plasma membrane and suggest how signalling chains might alter cell morphology.

    Article  CAS  Google Scholar 

  48. Baskin, T. I. On the alignment of cellulose microfibrils by cortical microtubules: a review and a model. Protoplasma 215, 150–171 (2001).

    Article  CAS  Google Scholar 

  49. Arioli, T. et al. Molecular analysis of cellulose biosynthesis in Arabidopsis. Science 279, 717–720 (1998).

    Article  CAS  Google Scholar 

  50. Sugimoto, K., Williamson, R. E. & Wasteneys, G. O. Wall architecture in the cellulose-deficient rsw1 mutant of Arabidopsis thaliana: microfibrils but not microtubules lose their transverse alignment before microfibrils become unrecognizable in the mitotic and elongation zones of roots. Protoplasma 215, 172–183 (2001).

    Article  CAS  Google Scholar 

  51. Gardiner, J. C., Taylor, N. G. & Turner, S. R. Control of cellulose synthase complex localization in developing xylem. Plant Cell 15, 1740–1748 (2003).

    Article  CAS  Google Scholar 

  52. Sugimoto, K., Himmelspach, R., Williamson, R. E. & Wasteneys, G. O. Mutation or drug-dependent microtubule disruption causes radial swelling without altering parallel cellulose microfibril deposition in Arabidopsis root cells. Plant Cell 15, 1414–1429 (2003). This work shows that the relationship between microtubules and cellulose alignment is far from simple.

    Article  CAS  Google Scholar 

  53. Wiedemeier, A. M. et al. Mutant alleles of Arabidopsis RADIALLY SWOLLEN 4 and 7 reduce growth anisotropy without altering the transverse orientation of cortical microtubules or cellulose microfibrils. Development 129, 4821–4830 (2002).

    CAS  PubMed  Google Scholar 

  54. McCartney, L., Steele-King, C. G., Jordan, E. & Knox, J. P. Cell wall pectic (1→4)-β-D-galactan marks the acceleration of cell elongation in the Arabidopsis seedling root meristem. Plant J. 33, 447–454 (2003).

    Article  CAS  Google Scholar 

  55. Park, S. K., Howden, R. & Twell, D. The Arabidopsis thaliana gametophytic mutation gemini pollen1 disrupts microspore polarity, division asymmetry and pollen cell fate. Development 125, 3789–3799 (1998).

    CAS  PubMed  Google Scholar 

  56. Mollinari, C. et al. PRC1 is a microtubule binding and bundling protein essential to maintain the mitotic spindle midzone. J. Cell Biol. 157, 1175–1186 (2002).

    Article  CAS  Google Scholar 

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Acknowledgements

The authors' work was supported by the Biotechnology and Biological Sciences Research Council (BBSRC) by way of a grant-in-aid to the John Innes Centre.

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Authors and Affiliations

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

    Clive Lloyd & Jordi Chan

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  1. Clive Lloyd
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Correspondence to Clive Lloyd.

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Related links

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DATABASES

LocusLink

katanin

phospholipase D

Swiss-Prot

CLIP170

EB1

KCM1

MAP65

MAP215

TAIR

bot1

FRA1

MOR1

rsw1

RSW4

RSW7

SPC98

FURTHER INFORMATION

'The Plant Cell' at ergito

Glossary

MICROTUBULE

A hollow tube, 25 nm in diameter, that is formed by the lateral association of (usually) 13 protofilaments, which are polymers of α- and β-tubulin subunits.

EXTRACELLULAR MATRIX

(ECM). The external coating of a cell. The plant cell's ECM — the cell wall — is mainly composed of various classes of complex carbohydrate that are structured around the fibrous polysaccharide, cellulose, whereas the main fibrous element of the animal cell's ECM is the protein collagen.

CENTROSOME

The main microtubule-organizing centre of animal cells.

FIBROBLAST

A common cell type that is found in the connective tissue in many parts of the body. Fibroblasts secrete an extracellular matrix that is rich in collagen and other macromolecules, and that connects cell layers.

CYTOPLASMIC STREAMING

The actomyosin-based movement of vesicles and organelles around the plant cell, on tracks that are provided by actin filaments.

MICROTUBULE-ASSOCIATED PROTEIN

A protein that, in the loosest sense, binds to microtubules. More stringently, it is a protein that co-purifies with microtubules in vitro.

INTERPHASE

The period between two mitotic divisions.

YEAST TWO-HYBRID APPROACH

A technique that is used to test if two proteins physically interact with each other. One protein is fused to the GAL4 activation domain and the other to the GAL4 DNA-binding domain, and both fusion proteins are introduced into yeast. The expression of a GAL4-regulated reporter gene indicates that the two proteins physically interact.

ORTHOLOGUES

A pair of genes, one in each species, that are descended from a single gene. If these two genes encode proteins with functional similarity they are referred to as functional orthologues.

INFLORESCENCE STEM

The stem that carries the flowers.

SECONDARY WALL

The flexible extracellular matrix that is deposited while the cell is still expanding is known as the primary cell wall. When expansion ceases, the secondary wall is laid down inside the primary wall, which makes it stronger.

ANISOTROPIC

Unlike isotropic growth, which occurs in all directions, anisotropic growth has a preferred direction.

KINESIN

A protein that uses the energy of ATP hydrolysis to move along a microtubule. Kinesins with the microtubule-binding domain at the amino-terminal head move cargo to the fast-growing plus end of the microtubule, whereas kinesins with motors at the carboxyl terminus move in the opposite direction.

CELL PLATE

The flattened disk of immature cell wall that is deposited by the fusion of Golgi vesicles in the plane where the two half sets of phragmoplast microtubules overlap. It contains a polysaccharide, callose, which is composed of chains of β-1,3-linked glucosyl residues.

HeLa CELLS

An established tissue-culture strain of human epidermoid carcinoma cells, which contain 70–80 chromosomes per cell. These cells were originally derived from tissue taken from a patient named Henrietta Lacks in 1951.

PHOTOBLEACHING

The irreversible destruction, by any one of several different mechanisms, of a fluorophore that is under illumination.

TAXOL

An antitumour agent that enhances the polymerization of tubulin and the subsequent stabilization of microtubules, thereby inhibiting mitosis and blocking the cell cycle.

CLADE

A taxon or other grouping of organisms consisting of a single species and its descendents.

TELOPHASE

The final stage of mitosis or meiosis in which the nuclei form in the daughter cells.

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Lloyd, C., Chan, J. Microtubules and the shape of plants to come. Nat Rev Mol Cell Biol 5, 13–23 (2004). https://doi.org/10.1038/nrm1277

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