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Crossed-Wires: Interactions and Cross-Talk Between the Microtubule and Microfilament Networks in Plants

  • David A. CollingsEmail author
Chapter
Part of the Plant Cell Monographs book series (CELLMONO, volume 11)

Abstract

In plant cells, the cytoskeleton comprises distinct and highly dynamic arrays of microtubules and actin microfilaments. The basic structures and proteins of both the microtubules (∼25  nm-diameter polymers of α- and β-tubulin heterodimers), and the microfilaments (∼7  nm-diameter polymers of 42 kDa actin monomers) are conserved in all eukaryotic organisms, and occur in all cell types. The third cytoskeletal array present in animal cells, intermediate filaments, are of a more varied composition and their presence has not (yet) been demonstrated in plant cells.

The basic organization of microtubules and microfilaments in various plant cells was determined over several decades from static images of fixed material. These images often demonstrated that microfilaments co-align with microtubules. As functional and molecular studies have become more prevalent, it has become apparent that co-ordination of dynamic microtubules and microfilaments is necessary for many facets of growth and development, and that cross-talk exists between them. Numerous studies have shown such interactions in animal cells (Gavin 1997; Goode et al. 2000; Dehmelt and Halpain 2003), and it is the diversity of these processes in plants that forms the subject of this review. As such, this review takes a broad approach to the topic. Defining microtubule–microfilament cross-talk (or microfilament–microtubule cross-talk for those of an actin persuasion) as any type of relationship between microtubules and microfilaments, the review commences with a reassessment of early work into colocalization between microtubules and microfilaments (Sect. ??), which leads to information about microtubule–microfilament interactions (Sect. ??). In this review, the term “interactions” implies a direct, physical relationship between the two components of the cytoskeleton, whereas “cross-talk” is used in a more encompassing way that includes indirect interactions. Section ??considers proteins that might mediate direct microtubule–microfilament interactions. However, taking the broad view of microtubule–microfilament cross-talk leads to discussion of systems where both microtubules and microfilaments play a role, but without any direct involvement with one another. Such microtubule–microfilament co-ordination seemingly occurs in organelle movement and shaping (Sect. ??). A further component of microtubule–microfilament cross-talk involves indirect, but specific interplay between the networks via the Rop-signalling pathway (Sect. ??).

The cytoskeleton performs numerous fundamental roles within plant cells, and plant biologists have demonstrated that the microtubules and microfilaments function independently in many of these. However, as this review documents, on the occasions when these two networks come together, and there is interplay between them, dissecting the tangled cross-wires of the microtubules and microfilaments can become difficult.

Keywords

Pollen Tube Root Hair Cortical Microtubule Cytoplasmic Streaming Pavement Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Abu-Abied M, Golomb L, Belausov E, Huang S, Geiger B, Kam Z, Staiger CJ, Sadot E (2006) Identification of plant cytoskeleton-interacting proteins by screening for actin stress fiber association in mammalian fibroblasts. Plant J 48:367–379 PubMedGoogle Scholar
  2. Ambrose JC, Li W, Marcus A, Ma H, Cyr R (2005) A minus-end directed kinesin with plus-end tracking protein activity is involved in spindle morphogenesis. Mol Biol Cell 16:1584–1592 PubMedGoogle Scholar
  3. Anderhag P, Hepler PK, Lazzaro MD (2000) Microtubules and microfilaments are both responsible for pollen tube elongation in the conifer Picea abies (Norway spruce). Protoplasma 214:141–157 Google Scholar
  4. Andersland JM, Dixon DC, Seagull RW, Triplett BA (1998) Isolation and characterization of cytoskeletons from cotton fiber cytoplasts. In Vitro Cell Dev Biol Plant 34:173–180 Google Scholar
  5. Baluška F, Wojtaszek P, Volkmann D, Barlow P (2003) The architecture of polarized cell growth: the unique status of elongating plant cells. BioEssays 25:569–576 PubMedGoogle Scholar
  6. Bannigan A, Baskin TI (2005) Directional cell expansion—turning toward actin. Curr Opin Plant Biol 8:619–624 PubMedGoogle Scholar
  7. Bannigan A, Wiedemeier AMD, Williamson RE, Overall RL, Baskin TI (2006) Cortical microtubule arrays lose uniform alignment between cells and are oryzalin resistant in the Arabidopsis mutant, radially swollen 6. Plant Cell Physiol 47:949–958 PubMedGoogle Scholar
  8. Barrero RA, Umeda M, Yamamura S, Uchimiya H (2002) Arabidopsis CAP regulates the actin cytoskeleton necessary for plant cell elongation and division. Plant Cell 14:149–163 PubMedGoogle Scholar
  9. Baskin TI, Bivens NJ (1995) Stimulation of radial expansion in Arabidopsis roots by inhibitors of actomyosin and vesicle secretion but not by various inhibitors of metabolism. Planta 197:514–521 PubMedGoogle Scholar
  10. Bibikova TN, Blancaflor EB, Gilroy S (1999) Microtubules regulate tip growth and orientation in root hairs of Arabidopsis thaliana. Plant J 17:657–665 PubMedGoogle Scholar
  11. Blancaflor EB (2000) Cortical actin filaments potentially interact with cortical microtubules in regulating polarity of cell expansion in primary roots of maize (Zea mays L.). J Plant Growth Regul 19:406–414 PubMedGoogle Scholar
  12. Blancaflor EB, Wang Y-S, Motes CM (2006) Organization and function of the actin cytoskeleton in developing root cells. Int Rev Cytol 252:219–264 PubMedGoogle Scholar
  13. Boevink P, Oparka K, Santa Cruz S, Martin B, Betteridge A, Hawes C (1998) Stacks on tracks: the plant Golgi apparatus traffics on an actin/ER network. Plant J 15:441–447 PubMedGoogle Scholar
  14. Brière C, Bordel A-C, Barthou H, Jauneau A, Steinmetz A, Alibert G, Petitprez M (2003) Is the LIM-domain protein HaWLIM1 associated with cortical microtubules in sunflower protoplasts? Plant Cell Physiol 44:1055–1063 PubMedGoogle Scholar
  15. Chen C, Marcus A, Li W, Hu Y, Vielle-Calzada J-P, Grossniklaus U, Cyr RJ, Ma H (2002) The Arabidopsis ATK1 gene is required for spindle morphogenesis in male meiosis. Development 129:2401–2409 PubMedGoogle Scholar
  16. Chu B, Kerr P, Carter JV (1993) Stabilizing microtubules with taxol increases microfilament stability during freezing of rye root tips. Plant Cell Environ 16:883–889 Google Scholar
  17. Chuong SDX, Franceschi VR, Edwards GE (2006) The cytoskeleton maintains organelle partitioning required for single-cell C4 photosynthesis in Chenopodiaceae species. Plant Cell 18:2207–2223 PubMedGoogle Scholar
  18. Chuong SDX, Good AG, Taylor GJ, Freeman MC, Moorhead GBG, Muench DG (2004) 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 PubMedGoogle Scholar
  19. Chuong SDX, Mullen RT, Muench DG (2002) Identification of a rice RNA- and microtubule-binding protein as the multifunctional protein (MFP), a peroxisomal enzyme involved in the β-oxidation of fatty acids. J Biol Chem 277:2419–2429 PubMedGoogle Scholar
  20. Cleary AL (1995) F-actin redistributions at the dividing site in living Tradescantia stomatal complexes as revealed by microinjection of rhodamine-phalloidin. Protoplasma 185:152–165 Google Scholar
  21. Clore AM, Dannenhoffer JM, Larkins BA (1996) EF-1α is associated with a cytoskeletal network surrounding protein bodies in maize endosperm cells. Plant Cell 8:2003–2014 PubMedGoogle Scholar
  22. Collings DA, Allen NS (2000) In: Staiger CJ, Baluška F, Volkmann D, Barlow PW (eds) Cortical actin interacts with the plasma membrane and microtubules. Actin: A Dynamic Framework for Multiple Plant Cell Functions. Kluwer Academic, Dordrecht, pp 145–163 Google Scholar
  23. Collings DA, Asada T, Allen NS, Shibaoka H (1998) Plasma membrane-associated actin in Bright Yellow 2 tobacco cells: Evidence for interaction with microtubules. Plant Physiol 118:917–928 PubMedGoogle Scholar
  24. Collings DA, Harper JDI, Vaughn KC (2003) The association of peroxisomes with the developing cell plate in dividing onion root cells depends on actin microfilaments and myosin. Planta 218:204–216 PubMedGoogle Scholar
  25. Collings DA, Lill AW, Himmelspach R, Wasteneys GO (2006) Drug sensitisation studies show actin microfilaments and microtubules interact during root elongation in Arabidopsis thaliana. New Phytol 170:275–290 PubMedGoogle Scholar
  26. Collings DA, Wasteneys GO (2005) Actin microfilament and microtubule distribution patterns in the expanding root of Arabidopsis thaliana. Can J Bot 83:579–590 Google Scholar
  27. Collings DA, Wasteneys GO, Williamson RE (1996) Actin-microtubule interactions in the alga Nitella: analysis of the mechanism by which microtubule depolymerization potentiates cytochalasin's effects on streaming. Protoplasma 191:178–190 Google Scholar
  28. Collings DA, Zsuppan G, Allen NS, Blancaflor EB (2001) Demonstration of prominent actin filaments in the root columella. Planta 212:392–403 PubMedGoogle Scholar
  29. Deeks MJ, Hussey PJ, Davies B (2002) Formins: intermediates in signal-transduction cascades that affect cytoskeletal reorganization. Trends Plant Sci 7:492–498 PubMedGoogle Scholar
  30. Dehmelt L, Halpain S (2003) Actin and microtubules in neurite initiation: are MAPs the missing link? J Neurobiol 58:18–33 Google Scholar
  31. Ding B, Turgeon R, Parthasarathy MV (1991a) Microfilament organization and distribution in freeze substituted tobacco plant tissues. Protoplasma 165:96–105 Google Scholar
  32. Ding B, Turgeon R, Parthasarathy MV (1991b) Microfilaments in the preprophase band of freeze substituted tobacco root cells. Protoplasma 165:209–211 Google Scholar
  33. Dong C-H, Kost B, Xia G, Chua N-H (2001a) Molecular identification and characterization of Arabidopsis AtADF1, AtADF5 and AtADF6 genes. Plant Mol Biol 45:517–527 PubMedGoogle Scholar
  34. Dong C-H, Xia G-X, Hong Y, Ramachandran S, Kost B, Chua N-H (2001b) ADF proteins are involved in the control of flowering and regulate F-actin organization, cell expansion, and organ growth in Arabidopsis. Plant Cell 13:1333–1346 PubMedGoogle Scholar
  35. Durso NA, Leslie JD, Cyr RJ (1996) In situ immunocytochemical evidence that a homolog of protein translation factor EF-1α is associated with microtubules in carrot cells. Protoplasma 190:141–150 Google Scholar
  36. Eleftheriou EP, Palevitz BA (1992) The effect of cytochalasin D on preprophase band organisation in root tip cells of Allium. J Cell Sci 103:989–998 Google Scholar
  37. Endow SA, Waligora KW (1998) Determinants of kinesin motor polarity. Science 281:1200–1202 PubMedGoogle Scholar
  38. Faix J, Grosse R (2006) Staying in shape with formins. Dev Cell 10:693–706 PubMedGoogle Scholar
  39. Foissner I (2004) Microfilaments and microtubules control the shape, motility, and subcellular distribution of cortical mitochondria in characean internodal cells. Protoplasma 224:145–157 PubMedGoogle Scholar
  40. Foissner I, Wasteneys GO (1999) Microtubules at wound sites of Nitella internodal cells passively co-align with actin bundles when exposed to hydrodynamic forces generated by cytoplasmic streaming. Planta 208:480–490 Google Scholar
  41. Foissner I, Wasteneys GO (2000) Microtubule disassembly enhances reversible cytochalasin-dependent disruption of actin bundles in characean internodes. Protoplasma 214:33–44 Google Scholar
  42. Frank MJ, Cartwright HN, Smith LG (2003) Three Brick genes have distinct functions in a common pathway promoting polarized cell division and cell morphogenesis in the maize leaf epidermis. Development 130:753–762 PubMedGoogle Scholar
  43. Franke WW, Herth W, van der Woude WJ, Morre DJ (1972) Tubular and filamentous structures in pollen tubes: possible involvement as guide elements in protoplasmic streaming and vectorial migration of secretory vesicles. Planta 105:317–341 Google Scholar
  44. Fu Y, Gu Y, Zheng Z, Wasteneys G, Yang Z (2005) Arabidopsis interdigitating cell growth requires two antagonistic pathways with opposing action on cell morphogenesis. Cell 120:687–700 PubMedGoogle Scholar
  45. Fu Y, Li H, Yang Z (2002) The ROP2 GTPase controls the formation of cortical fine F-actin and the early phase of directional cell expansion during Arabidopsis organogenesis. Plant Cell 14:777–794 PubMedGoogle Scholar
  46. Fu Y, Wu G, Yang Z (2001) Rop GTPase-dependent dynamics of tip-localized F-actin controls tip growth in pollen tubes. J Biol Chem 152:1019–1032 Google Scholar
  47. Gardiner JC, Harper JDI, Weerakoon ND, Collings DA, Ritchie S, Gilroy S, Cyr RJ, Marc J (2001) A 90-kD phospholipase D from tobacco binds to microtubules and the plasma membrane. Plant Cell 13:2143–2158 PubMedGoogle Scholar
  48. Gavin RH (1997) Microtubule–microfilament synergy in the cytoskeleton. Int Rev Cytol 173:207–242 PubMedCrossRefGoogle Scholar
  49. Gilliland LU, Pawloski LC, Kandasamy MK, Meagher RB (2003) Arabidopsis actin gene ACT7 plays an essential role in germination and root growth. Plant J 33:319–328 PubMedGoogle Scholar
  50. Gimona M, Djinovic-Carugo K, Kranewitter WJ, Winder SJ (2002) Functional plasticity of CH domains. FEBS Lett 513:98–106 PubMedGoogle Scholar
  51. Gimona M, Mital R (1998) The single CH domain of calponin is neither sufficient nor necessary for F-actin binding. J Cell Sci 111:1813–1821 PubMedGoogle Scholar
  52. Goode BL, Drubin DG, Barnes G (2000) Functional cooperation between the microtubule and actin cytoskeletons. Curr Op Cell Biol 12:63–71 PubMedGoogle Scholar
  53. Granger CL, Cyr RJ (2001) Use of abnormal preprophase bands to decipher division plane determination. J Cell Sci 114:599–607 PubMedGoogle Scholar
  54. Grebe M, Xu J, Möbius W, Ueda T, Nakano A, Geuze HJ, Rook MB, Scheres B (2003) Arabidopsis sterol endocytosis involves actin-mediated trafficking via ARA6-positive early endosomes. Curr Biol 13:1378–1387 PubMedGoogle Scholar
  55. Gu Y, Wang Z, Yang Z (2004) ROP/RAC GTPase: an old new master regulator for plant signaling. Curr Op Plant Biol 7:527–536 Google Scholar
  56. Gungabissoon RA, Khan S, Hussey PJ, Maciver SK (2001) Interaction of elongation factor 1α from Zea mays (ZmEF-1α) with F-actin and interplay with the maize actin severing protein, ZmADF3. Cell Motil Cytoskel 49:104–111 Google Scholar
  57. Gunning BES, Wick SM (1985) Preprophase bands, phragmoplasts and spatial control of cytokinesis. J Cell Sci Suppl 2:157–179 PubMedGoogle Scholar
  58. Hamada T, Igarashi H, Yao M, Hashimoto T, Shimmen T, Sonobe S (2006) Purification and characterization of plant dynamin from tobacco BY-2 cells. Plant Cell Physiol 47:1175–1181 PubMedGoogle Scholar
  59. Hardham AR, Green PB, Lang JM (1980) Reorganization of cortical microtubules and cellulose deposition during leaf formation in Graptopetalum paraguayense. Planta 149:181–195 Google Scholar
  60. Harper JDI, Weerakoon ND, Gardiner JC, Blackman LM, Marc J (2002) A 75-kDa plant protein isolated by tubulin-affinity chromatography is a peroxisomal matrix enzyme. Can J Bot 80:1018–1027 Google Scholar
  61. Hasezawa S, Nagata T (1993) Microtubule organizing centers in plant cells: localization of a 49 kDa protein that is immunologically cross-reactive to a 51 kDa protein from sea urchin centrosomes in synchronised tobacco BY-2 cells. Protoplasma 176:64–74 Google Scholar
  62. Hasezawa S, Sano T, Nagata T (1998) The role of microfilaments in the organization and orientation of microtubules during the cell cycle transition from M phase to G1 phase in tobacco BY-2 cells. Protoplasma 202:105–114 Google Scholar
  63. Holweg C, Nick P (2004) Arabidopsis myosin XI mutant is defective in organelle movement and polar auxin transport. Proc Nat Acad Sci USA 101:10488–10493 PubMedGoogle Scholar
  64. Huang S, An Y-Q, McDowell JM, McKinney EC, Meagher RB (1997) The Arabidopsis ACT11 actin gene is strongly expressed in tissues of the emerging inflorescence, pollen, and developing ovules. Plant Mol Biol 33:125–139 PubMedGoogle Scholar
  65. Hush JM, Overall RL (1992) Re-orientation of cortical F-actin is not necessary for wound-induced microtubule re-orientation and cell polarity establishment. Protoplasma 169:97–106 Google Scholar
  66. Hussey PJ, Hawkins TJ, Igarashi H, Kaloriti D, Smertenko A (2002) 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 PubMedGoogle Scholar
  67. Hussey PJ, Yuan M, Calder G, Khan S, Lloyd CW (1998) Microinjection of pollen-specific actin-depolymerizing factor, ZmADF1, reorientates F-actin strands in Tradescantia stamen hair cells. Plant J 14:353–357 Google Scholar
  68. Igarashi H, Orii H, Mori H, Shimmen T, Sonobe S (2000) Isolation of a novel 190 kDa protein from tobacco BY-2 cells: possible involvement in the interaction between actin filaments and microtubules. Plant Cell Physiol 41:920–931 PubMedGoogle Scholar
  69. Itano N, Hatano S (1991) F-actin bundling protein from Physarum polycephalum: purification and its capacity for co-bundling of actin filaments and microtubules. Cell Motil Cytoskel 19:244–254 Google Scholar
  70. Kakimoto T, Shibaoka H (1988) Cytoskeletal ultrastructure of phragmoplast-nuclei complexes isolated from cultured tobacco cells. Protoplasma Suppl 2:95–103 Google Scholar
  71. Ketelaar T, Allwood EG, Anthony RG, Voigt B, Menzel D, Hussey PJ (2004) The actin-interacting protein AIP1 is essential for actin organization and plant development. Curr Biol 14:145–149 PubMedGoogle Scholar
  72. Ketelaar T, de Ruijter NCA, Emons AMC (2003) Unstable F-actin specifies the area and microtubule direction of cell expansion in Arabidopsis root hairs. Plant Cell 15:285–292 PubMedGoogle Scholar
  73. Kobayashi H, Fukuda H, Shibaoka H (1988) Interrelation between the spatial disposition of actin filaments and microtubules during the differentiation of tracheary elements in cultured Zinnia cells. Protoplasma 143:29–37 Google Scholar
  74. Kong L-J, Hanley-Bowdoin L (2002) A geminivirus replication protein interacts with a protein kinase and a motor protein that display different expression patterns during plant development and infection. Plant Cell 14:1817–1832 PubMedGoogle Scholar
  75. Kost B, Spielhofer P, Chua N-H (1998) A GFP-mouse talin fusion protein labels plant actin filaments in vivo and visualizes the actin cytoskeleton in growing pollen tubes. Plant J 16:393–401 PubMedGoogle Scholar
  76. Kotzer AM, Wasteneys GO (2006) Mechanisms behind the puzzle: microtubule–microfilament cross-talk in pavement cell formation. Can J Bot 84:594–603 Google Scholar
  77. Kovar DR, Gibbon BC, McCurdy DW, Staiger CJ (2001) Fluorescently-labeled fimbrin decorates a dynamic actin filament network in live plant cells. Planta 213:390–395 PubMedGoogle Scholar
  78. Kropf DL, Bisgrove SR, Hable WE (1998) Cytoskeletal control of polar growth in plant cells. Curr Op Cell Biol 10:117–122 PubMedGoogle Scholar
  79. Kusner DJ, Barton JA, Qin C, Wang X, Iyer SS (2003) Evolutionary conservation of physical and functional interactions between phospholipase D and actin. Arch Biochem Biophys 412:231–241 PubMedGoogle Scholar
  80. Kwok EY, Hanson MR (2003) Microfilaments and microtubules control the morphology and movement of non-green plastids and stromules in Nicotiana tabacum. Plant J 35:16–26 PubMedGoogle Scholar
  81. Lancelle SA, Cresti M, Hepler PK (1987) Ultrastructure of the cytoskeleton in freeze-substituted pollen tubes of Nicotiana alata. Protoplasma 140:141–150 Google Scholar
  82. Lancelle SA, Hepler PK (1991) Association of actin with cortical microtubules revealed by immunogold localization in Nicotiana pollen tubes. Protoplasma 165:167–172 Google Scholar
  83. Lee Y-RJ, Giang HM, Liu B (2001) A novel plant kinesin-related protein specifically associates with the phragmoplast organelles. Plant Cell 13:2427–2439 PubMedGoogle Scholar
  84. Leung CL, Sun D, Zheng M, Knowles DR, Liem RKH (1999) Microtubule actin cross-linking factor (MACF): a hybrid of dystonin and dystrophin that can interact with the actin and microtubule cytoskeletons. J Cell Biol 147:1275–1285 PubMedGoogle Scholar
  85. Li S, Blanchoin L, Yang Z, Lord EM (2003) The putative Arabidopsis Arp2/3 complex controls leaf cell morphogenesis. Plant Physiol 132:2034–2044 PubMedGoogle Scholar
  86. Logan DC (2006) Plant mitochondrial dynamics. Bioch Biophys Acta 1763:430–441 Google Scholar
  87. Logan DC, Scott I, Tobin AK (2003) The genetic control of plant mitochondrial morphology and dynamics. Plant J 36:500–509 PubMedGoogle Scholar
  88. Lu L, Lee Y-RJ, Pan R, Maloof JN, Liu B (2005) 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 PubMedGoogle Scholar
  89. Mathur J, Mathur N, Kernebeck B, Hülskamp M (2003) Mutations in actin-related proteins 2 and 3 affect cell shape development in Arabidopsis. Plant Cell 15:1632–1645 PubMedGoogle Scholar
  90. Matsui K, Collings D, Asada T (2001) Identification of a novel plant-specific kinesin-like protein that is highly expressed in interphase tobacco BY-2 cells. Protoplasma 215:105–115 PubMedGoogle Scholar
  91. McCurdy DW, Gunning BES (1990) Reorganization of cortical actin microfilaments and microtubules at preprophase and mitosis in wheat root-tip cells: a double label immunofluorescence study. Cell Motil Cytoskel 15:76–87 Google Scholar
  92. Mineyuki Y, Palevitz BA (1990) Relationship between preprophase band organization, F-actin and the division site in Allium. J Cell Sci 97:283–295 Google Scholar
  93. Mitsui H, Nakatani K, Yamaguchi-Shinozaki K, Shinozaki K, Nishikawa K, Takahashi H (1994) Sequencing and characterization of the kinesin-related genes katB and katC of Arabidopsis thaliana. Plant Mol Biol 25:865–876 PubMedGoogle Scholar
  94. Mitsui H, Yamaguchi-Shinozaki K, Shinozaki K, Nishikawa K, Takahashi H (1993) Identification of a gene family (kat) encoding kinesin-like proteins in Arabidopsis thaliana and the characterization of secondary structure of KatA. Mol Gen Genet 238:362–368 PubMedGoogle Scholar
  95. Moore RC, Cyr RJ (2000) Association between elongation factor-1α and microtubules in vivo is domain dependent and conditional. Cell Motil Cytoskel 45:279–292 Google Scholar
  96. Moore RC, Durso NA, Cyr RJ (1998) Elongation factor-1α stabilizes microtubules in a calcium/calmodulin-dependent manner. Cell Motil Cytoskel 41:168–180 Google Scholar
  97. Motes CM, Pechter P, Yoo CM, Wang Y-S, Chapman KD, Blancaflor EB (2005) Differential effects of two phospholipase D inhibitors, 1-butanol and N-acylethanolamine, on in vivo cytoskeletal organization and Arabidopsis seedling growth. Protoplasma 226:109–123 PubMedGoogle Scholar
  98. Muday GK, Murphy AS (2002) An emerging model of auxin transport regulation. Plant Cell 14:293–299 PubMedGoogle Scholar
  99. Muench DG, Mullen RT (2003) Peroxisome dynamics in plant cells: a role for the cytoskeleton. Plant Sci 164:307–315 Google Scholar
  100. Nakasuka Y, Shimmen T (2006) The effects of microtubule inhibitors on actin cytoskeleton in root hairs of Limnobium. J Plant Res 119S:111 Google Scholar
  101. Narasimhulu SB, Reddy ASN (1998) Characterization of microtubule binding domains in the Arabidopsis kinesin-like calmodulin binding protein. Plant Cell 10:957–965 PubMedGoogle Scholar
  102. Nebenführ A, Gallagher LA, Dunahy TG, Frohlick JA, Mazurkiewicz AM, Meehl JB, Staehelin LA (1999) Stop-and-go movements of plant Golgi stacks are mediated by the acto-myosin system. Plant Physiol 121:1127–1141 PubMedGoogle Scholar
  103. Ni CZ, Wang HQ, Xu T, Qu Z, Liu GQ (2005) AtKP1, a kinesin-like protein, mainly localizes to mitochondria in Arabidopsis thaliana. Cell Res 15:725–733 PubMedGoogle Scholar
  104. Nishimura T, Yokota E, Wada T, Shimmen T, Okada K (2003) An Arabidopsis ACT2 dominant-negative mutation, which disturbs F-actin polymerization, reveals its distinctive function in root development. Plant Cell Physiol 44:1131–1140 PubMedGoogle Scholar
  105. Oliver TN, Berg JS, Cheney RE (1999) Tails on unconventional myosins. Cell Mol Life Sci 56:243–257 PubMedGoogle Scholar
  106. Oppenheimer DG, Pollock MA, Vacik J, Szymanski DB, Ericson B, Feldman K, Marks MD (1997) Essential role of a kinesin-like protein in Arabidopsis trichome morphogenesis. Proc Natl Acad Sci USA 94:6261–6266 PubMedGoogle Scholar
  107. Panteris E, Apostolakos P, Galatis B (1993) Microtubules and morphogenesis in ordinary epidermal cells of Vigna sinensis leaves. Protoplasma 174:91–100 Google Scholar
  108. Panteris E, Apostolakos P, Galatis B (2006) Cytoskeletal asymmetry in Zea mays subsidiary cell mother cells: a monopolar prophase microtubule half-spindle anchors the nucelus to its polar position. Cell Motil Cytoskel 63:696–709 Google Scholar
  109. Panteris E, Galatis B (2005) The morphogenesis of lobed plant cells in the mesophyll and epidermis: organization and distinct roles of cortical microtubules and actin filaments. New Phytol 167:721–732 PubMedGoogle Scholar
  110. Paredez AR, Somerville CR, Ehrhardt DW (2006) Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312:1491–1495 PubMedGoogle Scholar
  111. Preuss ML, Kovar DR, Lee Y-RJ, Staiger CJ, Delmer DP, Liu B (2004) A plant-specific kinesin binds to actin microfilaments and interacts with cortical microtubules in cotton fibers. Plant Physiol 136:3945–3955 PubMedGoogle Scholar
  112. Ramachandran S, Christensen HEM, Ishimaru Y, Dong C-H, Chao-Ming W, Cleary AL, Chua N-H (2000) Profilin plays a role in cell elongation, cell shape maintenance and flowering in Arabidopsis. Plant Physiol 124:1637–1647 PubMedGoogle Scholar
  113. Reddy ASN, Day IS (2001) Kinesins in the Arabidopsis genome: a comparative analysis among eukaryotes. BMC Genomics 2:2 PubMedGoogle Scholar
  114. Reddy ASN, Safadi F, Narasimhulu SB, Golovkin M, Hu X (1996) A novel plant calmodulin-binding protein with a kinesin heavy chain motor domain. J Biol Chem 271:7052–7060 PubMedGoogle Scholar
  115. Richardson DN, Simmons MP, Reddy ASN (2006) Comprehensive comparative analysis of kinesins in photosynthetic eukaryotes. BMC Genomics 7:18 PubMedGoogle Scholar
  116. Riesen D, Hanson MR (2007) Association of six YFP-myosin XI-tail fusions with mobile plant cell organelles. BMC Plant Biol 7:6 Google Scholar
  117. Romagnoli S, Cai G, Faleri C, Yokota E, Shimmen T, Cresti M (2007) Microtubule– and actin-filament-dependent motors are distributed on pollen tube mitochondria and contribute differently to their movement. Plant Cell Physiol 48:345–361 PubMedGoogle Scholar
  118. Saedler R, Mathur N, Srinivas BP, Kernebeck B, Hülskamp M, Mathur J (2004) Actin control over microtubules suggested by DISTORTED2 encoding the Arabidopsis ARPC2 subunit homolog. Plant Cell Physiol 45:813–822 PubMedGoogle Scholar
  119. Sano T, Higaki T, Oda Y, Hayashi T, Hasezawa S (2005) Appearance of actin microfilament twin peaks in mitosis and their function in cell plate formation, as visualized in tobacco BY-2 cells expressing GFP-fimbrin. Plant J 44:595–605 PubMedGoogle Scholar
  120. Sato Y, Wada M, Kadota A (2001) 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 PubMedGoogle Scholar
  121. Schwab B, Mathur J, Saedler R, Schwarz H, Frey B, Scheidegger C, Hülskamp M (2003) Regulation of cell expansion by the DISTORTED genes in Arabidopsis thaliana: actin controls the spatial organization of microtubules. Mol Gen Genomics 269:350–360 Google Scholar
  122. Seagull RW (1990) The effects of microtubule and microfilament disrupting agents on cytoskeletal arrays and wall deposition in developing cotton fibres. Protoplasma 159:44–59 Google Scholar
  123. Seagull RW (1992) A quantitative electron microscopic study of changes in microtubule arrays and wall microfibril orientation during in vitro cotton fiber development. J Cell Sci 101:561–577 Google Scholar
  124. Seagull RW, Heath IB (1979) The effects of tannic acid on the in vivo preservation of microfilaments. Eur J Cell Biol 20:184–188 PubMedGoogle Scholar
  125. Sheahan MB, McCurdy DW, Rose RJ (2005) Mitochondria as a connected population: ensuring continuity of the mitochondrial genome during plant cell dedifferentiation through massive mitochondrial fusion. Plant J 44:744–755 PubMedGoogle Scholar
  126. Sheahan MB, Staiger CJ, Rose RJ, McCurdy DW (2004) A green fluorescent protein fusion to actin-binding domain 2 of Arabidopsis thaliana fimbrin highlights new features of a dynamic actin cytoskeleton in live plant cells. Plant Physiol 136:3968–3978 PubMedGoogle Scholar
  127. Smith LG, Oppenheimer DG (2005) Spatial control of cell expansion by the plant cytoskeleton. Ann Rev Cell Dev Biol 21:271–295 Google Scholar
  128. Song H, Golovkin M, Reddy ASN, Endow SA (1997) In vitro motility of AtKCBP, a calmodulin-binding kinesin protein of Arabidopsis. Proc Natl Acad Sci USA 94:322–327 PubMedGoogle Scholar
  129. Sonobe S (1996) Studies on the plant cytoskeleton using miniprotoplasts of tobacco BY-2 cells. J Plant Res 109:437–448 Google Scholar
  130. Sonobe S, Shibaoka H (1989) Cortical fine actin filaments in higher plant cells visualized by rhodamine-phalloidin after pretreatment with m-maleimidobenzoyl N-hydroxysuccinimide ester. Protoplasma 148:80–86 Google Scholar
  131. Sutoh K (1984) Actin-actin and actin-deoxyribonuclease I contact sites in the actin sequence. Biochemistry 23:1942–1946 PubMedGoogle Scholar
  132. Takesue K, Shibaoka H (1998) The cyclic reorientation of cortical microtubules in epidermal cells of azuki bean epicotyls: the role of actin filaments in the progression of the cycle. Planta 205:539–546 PubMedGoogle Scholar
  133. Tamura K, Makatani K, Mitsui H, Ohashi Y, Takahashi H (1999) Characterization of katD, a kinesin-like protein gene specifically expressed in floral tissues of Arabidopsis thaliana. Gene 230:23–32 PubMedGoogle Scholar
  134. Thomas C, Hoffmann C, Dieterle M, van Troys M, Ampe C, Steinmetz A (2006) Tobacco WLIM1 is a novel F-actin binding proteins involved in actin cytoskeleton remodeling. Plant Cell 18:2194–2206 PubMedGoogle Scholar
  135. Timmers ACJ, Vallotton P, Heym C, Menzel D (2007) Microtubule dynamics in root hairs of Medicago truncatula. Eur J Cell Biol 86:69–83 PubMedGoogle Scholar
  136. Tiwari SC, Wick SM, Williamson RE, Gunning BES (1984) Cytoskeleton and integration of cellular function in cells of higher plants. J Cell Biol 99:63s-69s Google Scholar
  137. Tiwari SC, Wilkins TA (1995) Cotton (Gossypium hirsutum) seed trichomes expand via diffuse growing mechanism. Can J Bot 73:746–757 Google Scholar
  138. Tominaga M, Morita K, Sonobe S, Yokota E, Shimmen T (1997) Microtubules regulate the organization of actin filaments at the cortical region in root hair cells of Hydrocharis. Protoplasma 199:83–92 Google Scholar
  139. Traas JA, Doonan JH, Rawlins DJ, Shaw PJ, Watts J, Lloyd CW (1987) An actin network is present in the cytoplasm throughout the cell cycle of carrot cells and associates with the dividing nucleus. J Cell Biol 105:387–395 PubMedGoogle Scholar
  140. Ueda K, Matsuyama T (2000) Rearrangement of cortical microtubules from transverse to oblique or longitudinal in living cells of transgenic Arabidopsis thaliana. Protoplasma 213:28–38 Google Scholar
  141. van Gestel K, Köhler RH, Verbelen J-P (2002) 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 PubMedGoogle Scholar
  142. Vanstraelen M, Acosta JAT, De Veylder L, Inzé D, Geelen D (2004) A plant-specific subclass of C-terminal kinesins contains a conserved A-type cyclin-dependent kinase site implicated in folding and dimerization. Plant Physiol 135:1417–1429 PubMedGoogle Scholar
  143. Vanstraelen M, Inzé D, Geelen D (2006a) Mitosis-specific kinesins in Arabidopsis. Trends Plant Sci 11:167–175 PubMedGoogle Scholar
  144. Vanstraelen M, van Damme D, de Rycke R, Mylle E, Inzé D, Geelen D (2006b) Cell cycle-dependent targeting of a kinesin at the plasma membrane demarcates the division site in plant cells. Curr Biol 16:308–314 PubMedGoogle Scholar
  145. Wada M, Suetsugu N (2004) Plant organelle positioning. Curr Op Plant Biol 7:626–631 Google Scholar
  146. Waller F, Wang Q-Y, Nick P (2000) In: Staiger CJ, Baluška F, Barlow PW, Volkmann D (eds) Actin and signal-controlled cell elongation in coleoptiles. Actin: A Dynamic Framework for Multiple Plant Functions. Kluwer, Dordrecht, pp 477–496 Google Scholar
  147. Wang Q-Y, Nick P (1998) The auxin response of actin is altered in the rice mutant Yin-Yang. Protoplasma 204:22–33 PubMedGoogle Scholar
  148. Wang Y-S, Motes CM, Mohamalawari DR, Blancaflor EB (2004) Green fluorescent protein fusions to Arabidopsis fimbrin 1 for spatio-temporal imaging of F-actin dynamics in roots. Cell Motil Cytoskel 59:79–93 Google Scholar
  149. Wasteneys GO, Williamson RE (1991) Endoplasmic microtubules and nucleus-associated actin rings in Nitella internodal cells. Protoplasma 162:86–98 Google Scholar
  150. Wasteneys GO, Willingale-Theune J, Menzel D (1997) Freeze shattering: a simple and effective method for permeabilizing higher plant cell walls. J Microscopy 188:51–61 Google Scholar
  151. Wernicke W, Jung G (1992) Role of cytoskeleton in cell shaping of developing mesophyll of wheat (Triticum aestivum L.). Eur J Cell Biol 57:88–94 PubMedGoogle Scholar
  152. Whittington AT, Vugrek O, Wei KJ, Hasenbein NG, Sugimoto K, Rashbrooke MC, Wasteneys GO (2001) MOR1 is essential for organizing cortical microtubules in plants. Nature 411:610–613 PubMedGoogle Scholar
  153. Wilsen KL, Lovy-Wheeler A, Voigt B, Menzel D, Kunkel JG, Hepler PK (2006) Imaging the actin cytoskeleton in growing pollen tubes. Sex Plant Reprod 19:51–62 Google Scholar
  154. Wu G, Gu Y, Li S, Yang Z (2001) A genome-wide analysis of Arabidopsis Rop-interactive CRIB motif containing proteins that act as Rop GTPase targets. Plant Cell 13:2841–2856 PubMedGoogle Scholar
  155. Yang F, Demma M, Warren V, Dharmawardhane S, Condeelis J (1990) Identification of an actin-binding protein from Dictyostelium as elongation factor 1a. Nature 347:494–496 PubMedGoogle Scholar
  156. Yang W, Burkhart W, Cavallius J, Merrick WC, Boss WF (1993) Purification and characterization of a phosphatidylinositol 4-kinase activator in carrot cells. J Biol Chem 268:392–398 PubMedGoogle Scholar
  157. Yoneda A, Akatsuka M, Kumagai F, Hasezawa S (2004) Disruption of actin microfilaments causes cortical microtubule disorganization and extra-phragmoplast formation at M/G1 interface in synchronized tobacco cells. Plant Cell Physiol 45:761–769 PubMedGoogle Scholar
  158. Zhang D, Wadsworth P, Hepler PK (1993) Dynamics of microfilaments are similar, but distinct from microtubules during cytokinesis in living, dividing plant cells. Cell Motil Cytoskel 24:151–155 Google Scholar
  159. Zhang X, Dyachok J, Krishnakumar S, Smith LG, Oppenheimer DG (2005) IRREGULAR TRICHOME BRANCH1 in Arabidopsis encodes a plant homolog of the actin-related protein2/3 complex activator Scar/WAVE that regulates actin and microtubule organization. Plant Cell 17:2314–2326 PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2008

Authors and Affiliations

  1. 1.Plant Cell Biology Group, Research School of Biological SciencesAustralian National UniversityCanberraAustralia
  2. 2.Canterbury UniversityChristchurchNew Zealand

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