Review of the literature reveals that plant tubulins can undergo extensive phosphorylation by different types of protein kinases, and that phosphorylation on serine/threonine residues as well as at tyrosine residues can result in the generation of a high level of polymorphism of plant tubulin. Biochemical evidence is presented to demonstrate that phosphorylation of plant tubulin is controlled by different types of protein kinases. Because the phosphorylation sites can be located along the whole length of both the alpha and beta tubulins, it is possible that this type of post-translational modification in plants can participate in modulating the tubulin-tubulin interaction, interactions of tubulins with other proteins (including MAPs and proteins of other cytoskeletal structures), with the plasma membrane and in regulating the functional stability/instability of microtubular arrays. The possible effects of different types of tubulin phosphorylation on cell cycle progression in higher plants are discussed.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
J. S. Hyams and C. W. Lloyd, Microtubules (Alan R Liss, New York, 1994).
R. H. Goddard, S. M. Wick, C. D. Silflow, and D. P. Snustad, Microtubule components of plant cell cytoskeleton, Plant Physiol. 104, 1–6 (1994).
V. Baird, Y. B. Blume, and S. M. Wick, in: Plant Microtubules - Potential Targets for Biotechnological Applications, edited by P. Nick (Springer, Frankfurt/Berlin, 2000), pp. 155–187.
D. E. Fosket and L. C. Morejohn, Structural and functional organization of tubulin, Ann. Rev. Plant Physiol. Plant Mol. Biol. 43, 201–240 (1992).
P. J. Hussey, D. P. Snustad, and C. D. Silflow, in: The Cytoskeletal Basis of Plant Growth and Form, edited by C.W. Lloyd (Academic, London, 1991), pp. 15–27.
D. Breviario, Tubulin genes and promoters, in: Plant Microtubules - Potential Targets for Biotechnological Applications, edited by P. Nick (Springer, Frankfurt/Berlin, 2000), pp. 137–157.
S. D. Kopczak, N. A. Haas, P. J. Hussey, C. D. Silflow, and D. P. Snustad, The small genome of Arabidopsis contains at least six expressed α-tubulin genes, Plant Cell 4, 539–547 (1992).
R. B. Meagher and M. Fechheimer, in: The Arabidopsis Book (American Society of Plant Biologists, Rockville, MD, 2003), pp. 1–26.
D. P. Snustad, N. A. Haas, S. D. Kopczak, and C. D. Silflow, The small genome of Arabidopsis contains at least nine expressed β-tubulin genes, Plant Cell 4, 549–556 (1992).
R. F. Luduena, Multiple forms of tubulin: different gene products and covalent modifications, Int. Rev. Cytol. 178, 207–275 (1998).
T. H. MacRae, Tubulin post-translational modifications: enzymes and their mechanisms of action, Eur. J. Biochem. 244, 265–278 (1997).
S. Westermann and K. Weber, Post-translational modifications regulate microtubule function, Nature Rev. 4, 938–947 (2003).
D. Raybin and M. Flavin, An enzyme tyrosinating alpha-tubulin and its role in micro- tubule assembly, Biochem. Biophys. Res. Comm. 65, 1088–1095 (1975).
M. LeDizet and G. Piperno, Identification of an acetylation site of Chlamydomonas α- tubulin, Proc. Natl. Acad. Sci. USA 84, 5720–5724 (1987).
B. Edde, J. Rossier, J. P. Le Caer, E. Desbryeres, F. Gros, and P. Denoulet, Post- translational glutamylation of α-tubulin, Science 247, 83–85 (1990).
L. Paturle-Lafanechere, B. Edde, P. Denoulet, A. Van Dorsselaer, H. Mazarguil, J. P. Le Caer, J. Wehland, and D. Job, Characterization of a major tubulin variant which cannot be tyrosinated, Biochemistry 30, 10523–10528 (1991).
V. Redeker, N. Levilliers, J. M. Schmitter, J. P. Le Caer, J. Rossier, A. Adoutte, and M. H. Bre, Polyglycylation of tubulin: a posttranslational modification in axonemal microtubules, Science 266, 1688–1691 (1994).
J. M. Andreu and J. M. Pereda, Site-directed antibodies to tubulin. Cell Motil. Cytoskel. 26, 1–6 (1993).
A. Smertenko, Y. B. Blume, V. Viklicky, and P. Draber, Exposure of tubulin structural domains in Nicotiana tabacum microtubules probed by monoclonal antibodies, Eur. J. Cell Biol. 72, 104–112 (1997).
Y. B. Blume, A. Smertenko, N. N. Ostapets, V. Viklicky, and P. Draber, Post- translational modifications of plant tubulin, Cell Biol. Int. 21, 918–920 (1997).
J. Wehland, M. Schroeder, and K. Weber, Organization of microtubules in stabilized meristematic plant cells revealed by a rat monoclonal antibody reacting only with the tyrosinated form of α-tubulin, Cell Biol. Int. Rept. 8, 147–150 (1984).
P. J. Dawson and C. W. Lloyd, Identification of multiple tubulins in taxol microtubules purified from carrot suspension cells, EMBO J. 4, 2451–2455 (1985).
G. P. Kerr and J. V. Carter, Microtubules of higher plant contain acetylated α-tubulin, J. Cell Biol. 107, 670a (1988).
Y. B. Blume, B. V. Mikitsey, V. G. Solodushko, and N. N. Ostapets, Is the phos- phorylation possible mechanism of cytoskeleton reorganization in plant cells? in: Abstr Third Int. Congress Plant Mol. Biol. “Mol. Biol. of Plant Growth and Development” (Oct. 6–11, 1991, Tucson, AZ), p. 1082.
Y. B. Blume, V. G. Solodushko, N. N. Ostapets, and Y. Y. Gleba, The posttranslational modifications of tubulin as universal mechanism of microtubule reorganization: existence in plant cells, in: Abstr 5th Int. Congress Cell Biol. (July 26–31. 1992, Madrid), p. 72.
K. Mizuno, Induction of cold stability of microtubules in cultured tobacco cells, Plant Physiol. 100, 740–748 (1992).
J. Katsuta and H. Shibaoka, Inhibition by kinase inhibitors of the development and the disappearance of the preprophase band of microtubules in tobacco BY-2 cells, J. Cell Sci. 103, 397–405 (1992).
A. Nogami and Y. Minneyuki, Loosening of a preprophase band of microtubules in onion (Allium cepa L.) root tip cells by kinase inhibitors, Cell Struct. Funct. 24, 419–424 (1999).
S. M. Wolniak and P. M. Larsen, Changes in the metaphase transit times and the pattern of sister chromatid separation in stamen hair cells of Tradescantia after treatment with protein phosphatase inhibitors,J. Cell Sci. 102, 691–6715 (1992).
R. D. Smith, J. E. Wilson, J. C. Walker, and T. I. Baskin, Protein phosphatase inhibitors block root hair development and alter cell shape in Arabidopsis roots, Planta 194, 516– 524 (1994).
I. Foissner, F. Grolig, and G. Obermeyer, Reversible protein phosphorylation regulates the dynamic organization of pollen tube cytoskeleton: effects of calyculin A and okadaic acid, Protoplasma220, 1–15 (2002).
T. I. Baskin and J. E.Wilson, Inhibitors of protein kinases and phosphatases alter rootmorphology and disorganize cortical microtubules, Plant Physiol. 113, 493–502 (1997).
S. Hasezawa and T. Nagata, Okadaic acid as a probe to analyse the cell cycle progression in plant cells, Bot. Acta 105, 63–69 (1992).
K. Mizuno, Inhibition of gibberellin-induced elongation, reorientation of cortical microtubules and change of isoform of tubulin in epicotyl segments of azuki bean by protein kinase inhibitors, Plant Cell Physiol. 35, 1149–1157 (1994).
K. Zhang, Y. Tsukitani, and P. C. L. John, Mitotic arrest in tobacco caused by the phosphoprotein phosphatase inhibitor okadaic acid, Plant Cell Physiol. 33, 677–688 (1992).
R. J. Cyr, Calcium/calmodulin affects microtubule stability in lysed protoplasts, J. Cell Sci. 100, 311–317 (1991).
D. A. Koontz and J. H. Choi, Evidence for phosphorylation of tubulin in carrot suspension cells, Physiol. Plant. 87, 576–583 (1993).
L. Roef, E. Witters, J. Gadeyne, J. Marcussen, R. P. Newton, and H. A. Van Onckelen, Analysis of 3’,5’-cAMP and adenylyl cyclase activity in higher plants using polyclonal chicken egg yolk antibodies, Anal. Biochem. 233, 188–196 (1996).
H. Richards, S. Das, C. J. Smith, L. Pereira, A. Geisbrecht, N. J. Devitt, D. E. Games, J. Van Geyschem, A. G. Brenton, and R. P. Newton, Cyclic nucleotide content of tobacco BY-2 cells, Phytochemistry61, 531–537 (2002).
A. Moutinho, P. J. Hussey, A. J. Trewavas, and R. Malho, cAMP acts as a second messenger in pollen tube growth and reorientation, Proc. Natl. Acad. Sci. USA 98, 10481–10486 (2001).
D. Bridges, M. E. Fraser, and G. B. G. Moorhead, Cyclic nucleotide binding proteins in the Arabidopsis thaliana and Oryza sativa genomes, BMC Bioinformatics 6, 6 (2005).
A. Yemets, Y. Sheremet, and Y. B. Blume, Does tubulin phosphorylation correlate with cell death in plant cells? BMC Plant Biol. 5(Suppl 1), S36 (2005) doi:10.1186/1471-2229-5-S1-S36.
I. B. Gerber, K. Laukens, E. Witters, and I. A. Dubery, Lipopolysaccharide-responsive phosphoproteins in Nicotiana tabacum cells, Plant Physiol. Biochem. 44, 369–379(2006).
W.-P. Fang, C.-J. Jiang, M. Yu, A.-H. Ye, and Z.-X. Wang, Differentially expression of Tua1, a tubulin-encoding gene, during flowering of tea plant Camellia sinensis (L.) O. Kuntze using cDNA amplified fragment length polymorphism technique, Acta Biochim. Biophys. Sin., 38, 653–662 (2006).
S. M. Assmann, Cyclic AMP as a second messenger in higher plants: status and future prospects, Plant Physiol. 108, 885–889 (1995).
A. J. Trewavas, Plant cyclic AMP comes in from the cold, Nature 390, 657–658 (1997).
N. A. Durso and R. J. Cyr, A calmodulin-sensitive interaction between microtubules and a higher plant homolog of elongation factor-1 α, Plant Cell 6, 893–905 (1994).
C. Miege and E. Marechal, 1,2-sn-Diacylglycerol in plant cells: Product, substrate and regulator. Plant Physiol. Biochem. 37, 795–808 (1999).
V. Sundaresan and J. Colasanti, Cyclin-dependent kinases in higher plants: spatial and temporal control of cell division, in: Plant Cell Division, edited by D. Fransic, D. Dudits, and D. Inze (Portland Press, Portland, 1998), pp. 47–65.
L. Bogre, O. Calderini, P. Binarova, M. Mattauch, S. Till, S. Kiegerl, C. Jonak, C. Pollaschek, P Barker, N. S. Huskisson, H. Hirt, and E. Heberle-Bors, A MAP kinase is activated late in plant mitosis and becomes localized to the plane of cell division, Plant Cell 11, 101–114 (1999).
L. Bogre, I. Meskiene, E. Heberle-Bors, and H. Hirt, Stressing the role of MAP kinases in mitogenic stimulation, Plant Mol. Biol. 43, 705–718 (2000).
J. Doonan, Social controls on cell proliferation in plants, Curr. Opin. Plant Biol. 3, 482–487 (2000).
L. Cassimeris, Accessory protein regulation of microtubule dynamics throughout the cell cycle, Curr. Opin. Cell Biol. 11, 134–141 (1999).
J. Joubes, C. Chevalier, D. Dudits, E. Herberle-Bors, D. Inze, M. Umeda, and J. P. Renaudin, CDK-related protein kinases in plants, Plant Mol. Biol. 43, 607–620 (2000).
L. Bogre, K. Zwerger, I. Meskiene, P. Binarova, V. Csizmadia, C. Planck, E. Wagner, H. Hirt, and E. Heberle-Bors, The cdc2Ms kinase is differently regulated in the cytoplasm and in the nucleus, Plant Physiol. 113, 841–852 (1997).
A. Hemerly, J. A. Engler, C. Bergounioux, M. Van Montagu, G. Engler, D. Inzй, and P. Ferreira, Dominant negative mutants of the Cdc2 kinase uncouple cell division fromiterative plant development, EMBO J. 14, 3925–3936 (1995).
P. Binarova, J. Dolezel, P. Draber, E. Heberle-Bors, M. Strnad, and L. Bogre, Treatment of Vicia faba root tip cells with specific inhibitors to cyclin-dependent kinases leads to abnormal spindle formation, Plant J. 16, 697–707 (1998).
J. M. Healy, M. Menges, J. H. Doonan, and J. A. Murray, The Arabidopsis D-type cyclins CycD2 and CycD3 both interact in vivo with the PSTAIRE cyclin-dependent kinase Cdc2a but are differently controlled, J. Biol. Chem. 276, 7041–7047 (2000).
F. Roudier, E. Fedorova, J. Gyorgyey, F. Feher, S. Brown, A. Kondorosi, and E. Kondorosi, Cell cycle function of a Medicago sativa A2-type cyclin interacting with a PSTAIRE-type cyclin-dependent kinase and a retinoblastome protein, Plant J. 23, 73–83 (2000).
J. Doonan and P. Fobert, Conserved and novel regulators of the plant cell cycle, Curr. Opin. Cell Biol. 9, 824–830 (1997).
P. R. Fobert, V. Gaudin, P. Lunness, E. S. Coen, and J. H.Doonan, Distinct classes of cdc2-related genes are differentially expressed during the cell division cycle in plants, Plant Cell 8, 1465–1476 (1996).
J. Lee, A. Das, M. Yamaguchi, J. Hashimoto, N. Tsutsumi, Y. Uchimiya, and M. Umeda, Cell cycle function of a rice B2-type cyclin-dependent kinase. Plant J. 34, 417–425 (2003).
J. Colasanti, S. O. Cho, S. Wick, and V. Sundaresan, Localization of the functional p34cdc2 homologue of maize in root tip and stomatal complex cells: association with predicted division sites, Plant Cell. 5, 1101–1111 (1993).
T. Meszaros, P. Miskolczi, F. Ayaydin, A. Pettko-Szandtner, A. Peres, Z. Magyar, G. V. Horvath, L. Bako, A. Feher, and D. Dudits, Multiple cyclin-dependent kinase complexes and phosphatases control G2/M progression in alfalfa cells, Plant Mol. Biol. 43, 595–605 (2000).
Y. Mineyuki, The preprophase band of microtubules: its function as a cytokinetic apparatus in higher plants, Int. Rev. Cytol. 187, 1–49 (1999).
H. Stals, S. Bauwens, J. Traas, M. Van Montagu, G. Engler,and D. Inze, Plant CDC2 is not only targeted to the pre-prophase band, but also co-localizes with the spindle,phragmoplast, and chromosomes, FEBS Lett. 418, 229–234 (1997).
R. Hemsley, S. McCutcheon, J. Doonan, and C. Lloyd, P34(cdc2) kinase is associatedwith cortical microtubules from higher plant protoplasts, FEBS Lett. 508, 157–161 (2001).
F. Ayaydin, E. Vissi, T. Meszaros, P. Miskolczi, I. Kovacs, A. Feher, V. Dombradi, F. Erdodi, P. Gergely, and D. Dudits, Inhibition of serine/threonine-specific protein phosphatases causes premature activation of cdc2MsF kinase at G2/M transition and early mitotic microtubule organisation in alfalfa, Plant J. 23, 3985–3995 (2000).
J. M. Hush, L. Wu, P. C. L. John, L. H. Hepler, and P. K. Hepler, Plant mitosis promoting factors disassembles the microtubule preprophase band and accelerates prophase progression in Tradescantia, Cell Biol. Int. 20, 275–287 (1996).
T. Asada, R. Kuriyama, and H. Shibaoka, TKRP125, a kinesin-related protein involved in the centrosome-independent organization of the cytokinetic apparatus in tobacco BY-2 cells, J. Cell Sci. 110, 179–189 (1997).
O. Calderini, L. Bogre, O. Vicente, P. Binarova, E. Heberle-Bors, and C. Wilson, A cell cycle regulated MAP kinase with a possible role in cytokinesis in tobacco cells. J. Cell Sci. 111, 3091–3100 (1998).
M. Weingartner, P. Binarova, D. Drykova, A. Schweighofer, J. P. David, E. Heberle-Bors, J. Doonan, and L. Bogre, Dynamic recruitment of Cdc2 to specific tubule structures during mitosis, Plant Cell 13, 1929–1943 (2001).
S. P. Wheatley, E. H. Hinchcliffe, M. Glotzer, A. A. Hyman, G. Sluder, and Y. Wang, CDK1 inactivation regulates anaphase spindle dynamics and cytokinesis in vivo, J. Cell Biol. 138, 385–393 (1997).
A. Yemets, Y. Sheremet, K. Vissenberg, J. Van Orden, J. P. Verbelen, and Y. B. Blume, Effects of tyrosine kinase and phosphatase inhibitors on microtubules in Arabidopsis root cells, Cell Biol. Int. 32, (2008) doi:10.1016/j.cellbi.2008.01.013.
Y. B. Blume, A. I. Yemets, V. Viklicky, and P. Draber, Post-translational modifications of multiple tubulin (Tub) genes, Mol. Biol. Cell10, 141a (1999).
R. Tournebize, S. S. Andersen, F. Verde, M. Doree, E. Karsenti, and A. A. Hyman, Distinct roles of PP1 and PPA-like phosphatase in control of microtubule dynamics during mitosis, EMBO J. 16, 5537–5549 (1997).
A. Arundhati, H. Feiler, J. Traas, H. Zhang, P. A. Lunness, and J. H. Doonan, A novel Arabidopsis type 1 protein phosphatase is highly expressed in male and female tissues and functionally complements a conditional cell cycle mutant of Aspergillus, Plant J. 7, 823–834 (1995).
P. L. Rodriguez, M. P. Leube, and E. Grill, Molecular cloning in Arabidopsis thaliana of a new protein phosphatase 2C (PP2C) with homology to ABI1 and ABI2, Plant Mol. Biol. 38, 879–883 (1998).
O. S. Awotunde, K. Lechward, K. Krajewska, S. Zolnierowicz, and G. Muszynska, Interaction of maize (Zea mays) protein phosphatase 2A with tubulin, Acta Biochim. Polonica 50,131–138 (2003).
G.-W. Tian, D. Smith, S. Gluck, and T. I. Baskin, Higher plant cortical microtubule array analyzed in vitro in the presence of the cell wall, Cell Motil. Cytoskeleton 57, 26–36 (2004).
C. Camilleri, J. Azimzadeh, M. Pastuglia, C. Bellini, O. Grandjean, and D. Bouchez, The Arabidopsis TONNEAU2 gene encodes a putative novel protein phosphatase 2A regulatory subunit essential for the control of the cortical cytoskeleton, Plant Cell 14, 833–845 (2002).
K. Naoi and T. Hashimoto, A semidominant mutation in an Arabidopsis mitogen-activated protein kinase phosphatase-like gene compromises cortical microtubule organization, Plant Cell16, 1841–1853 (2004).
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2008 Springer Science + Business Media B.V.
About this paper
Cite this paper
Blume, Y.B., Lloyd, C.W., Yemets, A.I. (2008). Plant Tubulin Phosphorylation And Its Role In Cell Cycle Progression. In: Blume, Y.B., Baird, W.V., Yemets, A.I., Breviario, D. (eds) The Plant Cytoskeleton: a Key Tool for Agro-Biotechnology. NATO Science for Peace and Security Series C: Environmental Security. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-8843-8_7
Download citation
DOI: https://doi.org/10.1007/978-1-4020-8843-8_7
Publisher Name: Springer, Dordrecht
Print ISBN: 978-1-4020-8842-1
Online ISBN: 978-1-4020-8843-8
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)