Advertisement

The Microtubule Proteome: A Role in Regulating Protein Synthesis and Import Into Organelles?

  • Teagen D. Quilichini
  • Douglas G. Muench*
Conference paper
Part of the NATO Science for Peace and Security Series C: Environmental Security book series (NAPSC)

Microtubules (MTs) are dynamic components of plant cells, and are organized into four major arrays. The growth and organization of MTs in these arrays is regulated by a group of structural proteins called the microtubule-associated proteins (MAPs). A number of MAPs have been identified in plants, some of which are plant-specific. Another group of MT-binding proteins that are well represented in plants are the kinesin-related motor proteins. A third and more loosely defined group of proteins that bind to MTs are the MT-interacting proteins. Binding of these proteins to MTs can serve to concentrate the protein, to regulate the activity of the protein, or to serve other functions. Numerous putative MT-interacting proteins were identified in two large-scaled studies. A group of proteins that were represented in one of these studies were peroxisomal matrix proteins. The MT and RNA binding activity of these peroxisomal proteins has led to a model that links MTs to protein synthesis and targeting of these proteins to peroxisomes.

Keywords

Microtubule proteome translational control microtubule-interacting protein peroxisome 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    C. Lloyd and P. Hussey, Microtubule-associated proteins in plants: why we need a MAP, Nat. Rev. Mol. Cell. Biol. 2, 40 – 47 (2001).PubMedCrossRefGoogle Scholar
  2. 2.
    G. O. Wasteneys, Microtubule organization in the green kingdom: chaos or self-order? J. Cell Sci. 115, 1345 – 1354 (2002).PubMedGoogle Scholar
  3. 3.
    C. Lloyd and J. Chan, Microtubules and the shape of plants to come, Nat. Rev. Mol. Cell. Biol. 5, 13 – 22 (2004).PubMedCrossRefGoogle Scholar
  4. 4.
    A. R. Paredez, C. R. Somerville, and D. W. Ehrhardt, Visualization of cellulose synthase demonstrates functional association with microtubules, Science 312, 1491 – 1495 (2006).PubMedCrossRefGoogle Scholar
  5. 5.
    G. O. Wasteneys, Progress in understanding the role of microtubules in plant cells, Curr. Opin. Plant Biol. 7, 651 – 660 (2004).PubMedCrossRefGoogle Scholar
  6. 6.
    J. M. Hush, P. Wadsworth, D. A. Callaham, and P. K. Hepler, Quantification of microtubule dynamics in living plant cells using fluorescence redistribution after photobleaching, J. Cell Sci. 107 (Pt 4), 775 – 784 (1994).PubMedGoogle Scholar
  7. 7.
    S. L. Shaw, R. Kamyar, and D. W. Ehrhardt, Sustained microtubule treadmilling in Arabidopsis cortical arrays, Science 300, 1715 – 1718 (2003).PubMedCrossRefGoogle Scholar
  8. 8.
    M. Yuan, P. J. Shaw, R. M. Warn, and C. W. Lloyd, Dynamic reorientation of cortical microtubules, from transverse to longitudinal, in living plant cells, Proc. Natl. Acad. Sci. U.S.A. 91, 6050 – 6053 (1994).PubMedCrossRefGoogle Scholar
  9. 9.
    J. C. Sedbrook, MAPs in plant cells: delineating microtubule growth dynamics and organization, Curr. Opin. Plant Biol. 7, 632 – 640 (2004).PubMedCrossRefGoogle Scholar
  10. 10.
    C. Lloyd, C. Chan, and P. Hussey, in: The Plant Cytoskeleton in Cell Differentiation and Development, edited by P. J. Hussey (Blackwell, Oxford, 2004), pp. 3 – 31.Google Scholar
  11. 11.
    E. Mandelkow and E. M. Mandelkow, Microtubules and microtubule-associated proteins, Curr. Opin. Cell Biol. 7, 72 – 81 (1995).PubMedCrossRefGoogle Scholar
  12. 12.
    R. B. Maccioni and V. Cambiazo, Role of microtubule-associated proteins in the control of microtubule assembly, Physiol. Rev. 75, 835 – 864 (1995).PubMedGoogle Scholar
  13. 13.
    S. D. Chuong, A. G. Good, G. J. Taylor, M. C. Freeman, G. B. Moorhead, and D. G. Muench, Large-scale identification of tubulin-binding proteins provides insight on subcellular trafficking, metabolic channeling, and signaling in plant cells, Mol. Cell. Proteomics 3, 970 – 983 (2004).PubMedCrossRefGoogle Scholar
  14. 14.
    T. Hamada, Microtubule-associated proteins in higher plants, J. Plant Res. 120, 79 – 98 (2007).PubMedCrossRefGoogle Scholar
  15. 15.
    J. Gardiner and J. Marc, Putative microtubule-associated proteins from the Arabidopsis genome, Protoplasma 222, 61 – 74 (2003).PubMedCrossRefGoogle Scholar
  16. 16.
    R. B. Meagher and M. Fechheimer, in: The Arabidopsis Book, edited by C. R. Somerville and E. M. Meyerowitz (American Society of Plant Biologists, Rockville, MD, 2003).Google Scholar
  17. 17.
    A. V. Korolev, J. Chan, M. J. Naldrett, J. H. Doonan, and C. W. Lloyd, Identification of a novel family of 70 kDa microtubule-associated proteins in Arabidopsis cells, Plant J. 42, 547 – 555 (2005).PubMedCrossRefGoogle Scholar
  18. 18.
    L. Vickerman and D. G. Muench, in: Plant Proteomics: Technologies, Strategies and Applications, edited by R. Rakwal (Wiley Interscience, USA, 2008) 275 – 289.Google Scholar
  19. 19.
    J. C. Ambrose, T. Shoji, A. M. Kotzer, J. A. Pighin, and G. O. Wasteneys, The Arabidopsis CLASP gene encodes a microtubule-associated protein involved in cell expansion and division, Plant Cell 19, 2763 – 2775 (2007).PubMedCrossRefGoogle Scholar
  20. 20.
    V. Kirik, U. Herrmann, C. Parupalli, J. C. Sedbrook, D. W. Ehrhardt, and M. Hulskamp, CLASP localizes in two discrete patterns on cortical microtubules and is required for cell morphogenesis and cell division in Arabidopsis, J. Cell Sci. 120, 4416 – 4425 (2007).PubMedCrossRefGoogle Scholar
  21. 21.
    A. T. Whittington, O. Vugrek, K. J. Wei, N. G. Hasenbein, K. Sugimoto, M. C. Rashbrooke, and G. O. Wasteneys, MOR1 is essential for organizing cortical microtubules in plants, Nature 411, 610 – 613 (2001).PubMedCrossRefGoogle Scholar
  22. 22.
    R. Zhong, D. H. Burk, W. H. Morrison, 3rd, and Z. H. Ye, A kinesin-like protein is essential for oriented deposition of cellulose microfibrils and cell wall strength, Plant Cell 14, 3101 – 3117 (2002).PubMedCrossRefGoogle Scholar
  23. 23.
    R. J. Cyr and B. A. Palevitz, Microtubule-binding proteins from carrot 1. Initial characterization and microtubule bundling, Planta 177, 245 – 260 (1989).CrossRefGoogle Scholar
  24. 24.
    M. Vantard, P. Schellenbaum, A. Fellous, and A. M. Lambert, Characterization of maize microtubule-associated proteins, one of which is immunologically related to tau, Biochemistry 30, 9334 – 9340 (1991).PubMedCrossRefGoogle Scholar
  25. 25.
    C.-J. Jiang and S. Sonobe, Identification and preliminary characterization of a 65 kDa higher-plant microtubule-associated protein, J. Cell Sci. 105, 891–901 (1993).Google Scholar
  26. 26.
    M. Sasabe and Y. Machida, MAP65: a bridge linking a MAP kinase to microtubule turnover, Curr. Opin. Plant Biol. 9, 563–570 (2006).PubMedCrossRefGoogle Scholar
  27. 27.
    D. Van Damme, K. Van Poucke, E. Boutant, C. Ritzenthaler, D. Inze, and D. Geelen, In vivo dynamics and differential microtubule-binding activities of MAP65 proteins, Plant Physiol. 136, 3956–3967 (2004).PubMedCrossRefGoogle Scholar
  28. 28.
    A. V. Korolev, H. Buschmann, J. H. Doonan, and C. W. Lloyd, AtMAP70-5, a divergent member of the MAP70 family of microtubule-associated proteins, is required for anisotropic cell growth in Arabidopsis, J. Cell Sci. 120, 2241–2247 (2007).PubMedCrossRefGoogle Scholar
  29. 29.
    N. A. Durso and R. J. Cyr, A calmodulin-sensitive interaction between microtubules and a higher plant homolog of elongation factor-1a, Plant Cell 6, 893–905 (1994).PubMedCrossRefGoogle Scholar
  30. 30.
    K. A. Suprenant, L. B. Tempero, and L. E. Hammer, Association of ribosomes with in vitro assembled microtubules, Cell Motil. Cytoskel. 14, 401–415 (1989).CrossRefGoogle Scholar
  31. 31.
    J. Marc, D. E. Sharkey, N. A. Durso, M. Zhang, and R. J. Cyr, Isolation of a 90-kD Microtubule-Associated Protein from Tobacco Membranes, Plant Cell 8, 2127–2138 (1996).PubMedCrossRefGoogle Scholar
  32. 32.
    K. G. Miller, C. M. Field, B. M. Alberts, and D. R. Kellogg, Use of actin filament and microtubule affinity chromatography to identify proteins that bind to the cytoskeleton, Methods Enzymol. 196, 303–319 (1991).PubMedCrossRefGoogle Scholar
  33. 33.
    D. R. Kellogg, C. M. Field, and B. M. Alberts, Identification of microtubule-associated proteins in the centrosome, spindle, and kinetochore of the early Drosophila embryo, J. Cell Biol. 109, 2977–2991 (1989).PubMedCrossRefGoogle Scholar
  34. 34.
    N. Balaban and R. Goldman, Isolation and characterization of a unique 15 kilodalton trypanosome subpellicular microtubule-associated protein, Cell Motil. Cytoskeleton 21, 138–146 (1992).PubMedCrossRefGoogle Scholar
  35. 35.
    S. D. X. Chuong, R. Mullen, and D. G. Muench, Identification of a rice RNA- and MTbinding protein as the multifunctional protein (MFP), a peroxisomal enzyme involved in the b-oxidation of fatty acids, J. Biol. Chem. 277, 2419–2429 (2002).PubMedCrossRefGoogle Scholar
  36. 36.
    J. C. Gardiner, J. D. I. Harper, N. D. Weerakoon, D. A. Collings, S. Ritchie, S. Gilroy, R. J. Cyr, and J. Marc, A 90-kD phospholipase D from tobacco binds to microtubules and the plasma membrane, Plant Cell 13, 2143– 2158 (2001).PubMedCrossRefGoogle Scholar
  37. 37.
    P. Dhonukshe, A. M. Laxalt, J. Goedhart, T. W. Gadella, and T. Munnik, Phospholipased activation correlates with microtubule reorganization in living plant cells, Plant Cell 15, 2666– 2679 (2003).PubMedCrossRefGoogle Scholar
  38. 38.
    J. Gardiner, D. A. Collings, J. D. Harper, and J. Marc, The effects of the phospholipase D-antagonist 1-butanol on seedling development and microtubule organisation in Arabidopsis, Plant Cell Physiol. 44, 687– 696 (2003).PubMedCrossRefGoogle Scholar
  39. 39.
    R. C. Moore and R. J. Cyr, Association between elongation factor-1alpha and microtubules in vivo is domain dependent and conditional, Cell Motil. Cytoskeleton 45, 279– 292 (2000).PubMedCrossRefGoogle Scholar
  40. 40.
    S. D. Chuong, R. T. Mullen, and D. G. Muench, The peroxisomal multifunctional protein interacts with cortical microtubules in plant cells, BMC Cell Biol. 6, 40 (2005).PubMedCrossRefGoogle Scholar
  41. 41.
    H. Buschmann, J. Chan, L. Sanchez-Pulido, M. A. Andrade-Navarro, J. H. Doonan, and C. W. Lloyd, Microtubule-associated AIR9 recognizes the cortical division site at preprophase and cell-plate insertion, Curr. Biol. 16, 1938– 1943 (2006).PubMedCrossRefGoogle Scholar
  42. 42.
    A. P. Smertenko, H. Y. Chang, S. Sonobe, S. I. Fenyk, M. Weingartner, L. Bogre, and P. J. Hussey, Control of the AtMAP65-1 interaction with microtubules through the cell cycle, J. Cell Sci. 119, 3227– 3237 (2006).PubMedCrossRefGoogle Scholar
  43. 43.
    R.-P. Jansen, mRNA localization: message on the move, Nat. Rev. Mol. Cell. Biol. 2, 247 – 256 (2001).PubMedCrossRefGoogle Scholar
  44. 44.
    Z. Elisha, L. Havin, I. Ringel, and J. K. Yisraei, Vg1 RNA binding protein mediates the association of Vg1 RNA with microtubules in Xenopus oocytes., EMBO J. 14, 5109 – 5114 (1995).PubMedGoogle Scholar
  45. 45.
    J. O. Deshler, M. I. Highett, T. Abramson, and B. Schnapp, A highly conserved RNA-binding protein for cytoplasmic mRNA localization in vertebrates, Curr. Biol. 8, 489 – 496 (1997).CrossRefGoogle Scholar
  46. 46.
    L. Wickham, T. Duchaîne, M. Luo, I. R. Nabi, and L. DesGroseillers, Mammalian staufen is a double-stranded-RNA and tubulin-binding protein which localizes to the rough endoplasmic reticulum, Mol. Cell Biol. 19, 2220 – 2230 (1999).PubMedGoogle Scholar
  47. 47.
    R.-P. Jansen, RNA-cytoskeletal associations, FASEB J 13, 455 – 466 (1999).PubMedGoogle Scholar
  48. 48.
    D. G. Muench and N. I. Park, Messages on the move: the role of the cytoskeleton in mRNA localization and translation in plant cells, Can. J. Bot. 84, 572 – 580 (2006).CrossRefGoogle Scholar
  49. 49.
    X. Li, V. R. Franceschi, and T. W. Okita, Segregation of storage protein mRNAs on the rough endoplasmic reticulum membranes of rice endosperm cells, Cell 72, 869 – 879 (1993).PubMedCrossRefGoogle Scholar
  50. 50.
    D. G. Muench, Y. Wu, S. J. Coughlan, and T. W. Okita, Evidence for a cytoskeleton-associated binding site involved in prolamine mRNA localization to the protein bodies in rice endosperm tissue, Plant Physiol. 116, 559 – 569 (1998).PubMedCrossRefGoogle Scholar
  51. 51.
    S. Hamada, K. Ishiyama, S. B. Choi, C. Wang, S. Singh, N. Kawai, V. R. Franceschi, and T. W. Okita, The transport of prolamine RNAs to prolamine protein bodies in living rice endosperm cells, Plant Cell 15, 2253 – 2264 (2003).PubMedCrossRefGoogle Scholar
  52. 52.
    J. Lane and V. Allan, Microtubule-based membrane movement, Biochim. Biophys. Acta 1376, 27 – 55 (1998).PubMedGoogle Scholar
  53. 53.
    M. Wada and N. Suetsugu, Plant organelle positioning, Curr. Opin. Plant Biol. 7, 626 – 631 (2004).PubMedCrossRefGoogle Scholar
  54. 54.
    C. R. Hawes and B. Satiat-Jeunemaitre, Trekking along the cytoskeleton, Plant Physiol. 125, 119 – 122 (2001).PubMedCrossRefGoogle Scholar
  55. 55.
    K. Van Gestel, R. H. Kohler, and J. P. Verbelen, Plant mitochondria move on F-actin, but their positioning in the cortical cytoplasm depends on both F-actin and microtubules, J. Exp. Bot. 53, 659 – 667 (2002).PubMedCrossRefGoogle Scholar
  56. 56.
    P. Boevink, K. Oparka, S. Santa Cruz, B. Martin, A. Betteridge, and C. Hawes, Stacks on tracks: the plant Golgi apparatus traffics on an actin/ER network, Plant J. 15, 441 – 447 (1998).PubMedCrossRefGoogle Scholar
  57. 57.
    D. G. Muench and R. T. Mullen, Peroxisome dynamics in plant cells: a role for the cytoskeleton, Plant Sci. 164, 307 – 315 (2003).CrossRefGoogle Scholar
  58. 58.
    A. Nebenfuhr, L. A. Gallagher, T. G. Dunahay, J. A. Frohlick, A. M. Mazurkiewicz, J. B. Meehl, and L. A. Staehelin, Stop-and-go movements of plant Golgi stacks are mediated by the acto- myosin system, Plant Physiol. 121, 1127 – 1142. (1999).PubMedCrossRefGoogle Scholar
  59. 59.
    M. K. Kandasamy and R. B. Meagher, Actin-organelle interaction: association with chloroplast in arabidopsis leaf mesophyll cells, Cell Motil. Cytoskeleton 44, 110 – 118 (1999).PubMedCrossRefGoogle Scholar
  60. 60.
    L. Lu, Y. R. Lee, R. Pan, J. N. Maloof, and B. Liu, An internal motor kinesin is associated with the Golgi apparatus and plays a role in trichome morphogenesis in Arabidopsis, Mol. Biol. Cell 16, 811 – 823 (2005).PubMedCrossRefGoogle Scholar
  61. 61.
    E. Y. Kwok and M. R. Hanson, Microfilaments and microtubules control the morphology and movement of non-green plastids and stromules in Nicotiana tabacum, Plant J. 35, 16 – 26 (2003).PubMedCrossRefGoogle Scholar
  62. 62.
    Y. Sato, M. Wada, and A. Kadota, Choice of tracks, microtubules and/or actin filaments for chloroplast photo-movement is differentially controlled by phytochrome and a blue light receptor, J. Cell Sci. 114, 269 – 279 (2001).PubMedGoogle Scholar
  63. 63.
    I. Foissner, Microfilaments and microtubules control the shape, motility, and subcellular distribution of cortical mitochondria in characean internodal cells, Protoplasma 224, 145 – 157 (2004).PubMedCrossRefGoogle Scholar
  64. 64.
    Y. R. Lee, H. M. Giang, and B. Liu, A novel plant kinesin-related protein specifically associates with the phragmoplast organelles, Plant Cell 13, 2427 – 2439 (2001).PubMedCrossRefGoogle Scholar
  65. 65.
    S. L. Gupton, D. A. Collings, and N. S. Allen, Endoplasmic reticulum targeted GFP reveals ER organization in tobacco NT-1 cells during cell division, Plant Physiol. Biochem. 44, 95 – 105 (2006).PubMedCrossRefGoogle Scholar
  66. 66.
    M. Garcia, X. Darzacq, T. Delaveau, L. Jourdren, R. H. Singer, and C. Jacq, Mitochondria-associated yeast mRNAs and the biogenesis of molecular complexes, Mol. Biol. Cell 18, 362 – 368 (2007).PubMedCrossRefGoogle Scholar
  67. 67.
    S. Subramani, Hitchhiking fads en route to peroxisomes, J. Cell Biol. 156, 415 – 417. (2002).PubMedCrossRefGoogle Scholar
  68. 68.
    J. D. I. Harper, N. D. Weerakoon, J. C. Gardiner, L. M. Blackman, and J. Marc, A 75-kDa plant protein isolated by tubulin-affinity chromatography is a peroxisomal matrix enzyme, Can. J. Bot. 80, 1018 – 1027 (2002).CrossRefGoogle Scholar
  69. 69.
    X. Liu, B. Reig, I. M. Nasrallah, and P. J. Stover, Human cytoplasmic serine hydroxymethyltransferase is an mRNA binding protein, Biochemistry 39, 11523 – 11531 (2000).PubMedCrossRefGoogle Scholar
  70. 70.
    N. Tai, J. C. Schmitz, J. Liu, X. Lin, M. Bailly, T. M. Chen, and E. Chu, Translational autoregulation of thymidylate synthase and dihydrofolate reductase, Front Biosci. 9, 2521 – 2526 (2004).PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science + Business Media B.V. 2008

Authors and Affiliations

  • Teagen D. Quilichini
    • 1
  • Douglas G. Muench*
    • 1
  1. 1.Department of Biological SciencesUniversity of CalgaryCalgaryCanada

Personalised recommendations