Advertisement

The Preprophase Band and Division Site Determination in Land Plants

  • Yann Duroc
  • David Bouchez
  • Martine Pastuglia
Chapter
Part of the Advances in Plant Biology book series (AIPB, volume 2)

Abstract

In land plants, division plane is determined pre-mitotically, during the transition from G2 to M phase. A conspicuous spatial landmark of division plane determination is a narrow cortical band of microtubules, the preprophase band (PPB), a transient, premitotic array which precisely predicts the cortical region reached by the growing cell plate during cytokinesis. However, cells preparing for division exhibit a number of other cytological features contributing to division site establishment, such as nuclear migration, cytoplasmic modifications, and intra-cytoplasmic cytoskeleton reorganization. The spatial control of division plane is tightly linked to the temporal control of cell division by the cell cycle machinery. In this chapter, we review and discuss recently discovered cellular events and molecular partners potentially involved in division plane establishment and PPB function in land plants.

Keywords

Land Plant Division Plane Golgi Stack Cell Cycle Machinery Preprophase Band 
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.

References

  1. 1.
    Abdel-Ghany SE, Day IS, Simmons MP, Kugrens P, Reddy AS (2005) Origin and evolution of kinesin-like calmodulin-binding protein. Plant Physiol 138:1711–1722PubMedCrossRefGoogle Scholar
  2. 2.
    Allard JF, Wasteneys GO, Cytrynbaum EN (2010) Mechanisms of self-organization of cortical microtubules in plants revealed by computational simulations. Mol Biol Cell 21:278–286PubMedCrossRefGoogle Scholar
  3. 3.
    Ambrose JC, Cyr R (2007) The kinesin ATK5 functions in early spindle assembly in Arabidopsis. Plant Cell 19:226–236PubMedCrossRefGoogle Scholar
  4. 4.
    Ambrose JC, Cyr R (2008) Mitotic spindle organization by the preprophase band. Mol Plant 1:950–960PubMedCrossRefGoogle Scholar
  5. 5.
    Ambrose JC, Cyr R (2008) Mitotic spindle assembly and function. In: Verma DPS, Hong Z (eds) Plant cell monographs, vol. 9 cell division control in plants. Springer, Berlin, pp 141–167CrossRefGoogle Scholar
  6. 6.
    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 16:1584–1592PubMedCrossRefGoogle Scholar
  7. 7.
    Ambrose JC, Shoji T, Kotzer AM, Pighin JA, Wasteneys GO (2007) The Arabidopsis CLASP gene encodes a microtubule-associated protein involved in cell expansion and division. Plant Cell 19:2763–2775PubMedCrossRefGoogle Scholar
  8. 8.
    Ambrose JC, Wasteneys GO (2008) CLASP modulates microtubule-cortex interaction during self-organization of acentrosomal microtubules. Mol Biol Cell 19:4730–4737PubMedCrossRefGoogle Scholar
  9. 9.
    Asada T, Kuriyama R, Shibaoka H (1997) TKRP125, a kinesin-related protein involved in the centrosome-independent organization of the cytokinetic apparatus in tobacco BY-2 cells. J Cell Sci 110:179–189PubMedGoogle Scholar
  10. 10.
    Ayaydin F, Vissi E, Meszaros T, Miskolczi P, Kovacs I, Feher A, Dombradi V, Erdodi F, Gergely P, Dudits D (2000) 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 23:85–96PubMedCrossRefGoogle Scholar
  11. 11.
    Azimzadeh J, Nacry P, Christodoulidou A, Drevensek S, Camilleri C, Amiour N, Parcy F, Pastuglia M, Bouchez D (2008) Arabidopsis TONNEAU1 proteins are essential for preprophase band formation and interact with centrin. Plant Cell 20:2146–2159PubMedCrossRefGoogle Scholar
  12. 12.
    Bannigan A, Lizotte-Waniewski M, Riley M, Baskin TI (2008) Emerging molecular mechanisms that power and regulate the anastral mitotic spindle of flowering plants. Cell Motil Cytoskeleton 65:1–11PubMedCrossRefGoogle Scholar
  13. 13.
    Barroso C, Chan J, Allan V, Doonan J, Hussey P, Lloyd C (2000) Two kinesin-related proteins associated with the cold-stable cytoskeleton of carrot cells: characterization of a novel kinesin, DcKRP120-2. Plant J 24:859–868PubMedCrossRefGoogle Scholar
  14. 14.
    Binarova P, Dolezel J, Draber P, Heberle-Bors E, Strnad M, Bogre L (1998) Treatment of Vicia faba root tip cells with specific inhibitors to cyclin-dependent kinases leads to abnormal spindle formation. Plant J 16:697–707PubMedCrossRefGoogle Scholar
  15. 15.
    Bisgrove SR, Lee YR, Liu B, Peters NT, Kropf DL (2008) The microtubule plus-end binding protein EB1 functions in root responses to touch and gravity signals in Arabidopsis. Plant Cell 20:396–410PubMedCrossRefGoogle Scholar
  16. 16.
    Boruc J, Mylle E, Duda M, De Clercq R, Rombauts S, Geelen D, Hilson P, Inze D, Van Damme D, Russinova E (2009) Systematic localization of the Arabidopsis core cell cycle proteins reveals novel cell division complexes. Plant Physiol 152:553–565PubMedCrossRefGoogle Scholar
  17. 17.
    Boudolf V, Barroco R, Engler JD, Verkest A, Beeckman T, Naudts M, Inze D, De Veylder L (2004) B1-type cyclin-dependent kinases are essential for the formation of stomatal complexes in Arabidopsis thaliana. Plant Cell 16:945–955PubMedCrossRefGoogle Scholar
  18. 18.
    Boudolf V, Inze D, De Veylder L (2006) What if higher plants lack a CDC25 phosphatase? Trends Plant Sci 11:474–479PubMedCrossRefGoogle Scholar
  19. 19.
    Bowser J, Reddy AS (1997) Localization of a kinesin-like calmodulin-binding protein in dividing cells of Arabidopsis and tobacco. Plant J 12:1429–1437PubMedCrossRefGoogle Scholar
  20. 20.
    Brown RC, Lemmon BE (1990) Monoplastidic cell-division in lower land plants. Am J Bot 77:559–571CrossRefGoogle Scholar
  21. 21.
    Brown RC, Lemmon BE (2001) The cytoskeleton and spatial control of cytokinesis in the plant life cycle. Protoplasma 215:35–49PubMedCrossRefGoogle Scholar
  22. 22.
    Buschmann H, Chan J, Sanchez-Pulido L, Andrade-Navarro MA, Doonan JH, Lloyd CW (2006) Microtubule-associated AIR9 recognizes the cortical division site at preprophase and cell-plate insertion. Curr Biol 16:1938–1943PubMedCrossRefGoogle Scholar
  23. 23.
    Buschmann H, Fabri CO, Hauptmann M, Hutzler P, Laux T, Lloyd CW, Schaffner AR (2004) Helical growth of the Arabidopsis mutant tortifolia1 reveals a plant-specific microtubule-associated protein. Curr Biol 14:1515–1521PubMedCrossRefGoogle Scholar
  24. 24.
    Caillaud MC, Lecomte P, Jammes F, Quentin M, Pagnotta S, Andrio E, de Almeida Engler J, Marfaing N, Gounon P, Abad P, Favery B (2008) MAP65-3 microtubule-associated protein is essential for nematode-induced giant cell ontogenesis in Arabidopsis. Plant Cell 20:423–437PubMedCrossRefGoogle Scholar
  25. 25.
    Camilleri C, Azimzadeh J, Pastuglia M, Bellini C, Grandjean O, Bouchez D (2002) The Arabidopsis TONNEAU2 gene encodes a putative novel protein phosphatase 2A regulatory subunit essential for the control of the cortical cytoskeleton. Plant Cell 14:833–845PubMedCrossRefGoogle Scholar
  26. 26.
    Carazo-Salas RE, Gruss OJ, Mattaj IW, Karsenti E (2001) Ran-GTP coordinates regulation of microtubule nucleation and dynamics during mitotic-spindle assembly. Nat Cell Biol 3:228–234PubMedCrossRefGoogle Scholar
  27. 27.
    Chan J, Calder G, Fox S, Lloyd C (2005) Localization of the microtubule end binding protein EB1 reveals alternative pathways of spindle development in Arabidopsis suspension cells. Plant Cell 17:1737–1748PubMedCrossRefGoogle Scholar
  28. 28.
    Chan J, Calder GM, Doonan JH, Lloyd CW (2003) EB1 reveals mobile microtubule nucleation sites in Arabidopsis. Nat Cell Biol 5:967–971PubMedCrossRefGoogle Scholar
  29. 29.
    Chan J, Jensen CG, Jensen LC, Bush M, Lloyd CW (1999) The 65-kDa carrot microtubule-associated protein forms regularly arranged filamentous cross-bridges between microtubules. Proc Natl Acad Sci USA 96:14931–14936PubMedCrossRefGoogle Scholar
  30. 30.
    Chang HY, Smertenko AP, Igarashi H, Dixon DP, Hussey PJ (2005) Dynamic interaction of NtMAP65-1a with microtubules in vivo. J Cell Sci 118:3195–3201PubMedCrossRefGoogle Scholar
  31. 31.
    Chen C, Marcus A, Li W, Hu Y, Calzada JP, Grossniklaus U, Cyr RJ, Ma H (2002) The Arabidopsis ATK1 gene is required for spindle morphogenesis in male meiosis. Development 129:2401–2409PubMedCrossRefGoogle Scholar
  32. 32.
    Chytilova E, Macas J, Sliwinska E, Rafelski SM, Lambert GM, Galbraith DW (2000) Nuclear dynamics in Arabidopsis thaliana. Mol Biol Cell 11:2733–2741PubMedGoogle Scholar
  33. 33.
    Ciciarello M, Mangiacasale R, Lavia P (2007) Spatial control of mitosis by the GTPase Ran. Cell Mol Life Sci 64:1891–1914PubMedCrossRefGoogle Scholar
  34. 34.
    Cleary AL, Gunning BES, Wasteneys GO, Hepler PK (1992) Microtubule and F-actin dynamics at the division site in living Tradescantia stamen hair cells. J Cell Sci 103:977–988Google Scholar
  35. 35.
    Cleary AL, Smith LG (1998) The Tangled1 gene is required for spatial control of cytoskeletal arrays associated with cell division during maize leaf development. Plant Cell 10:1875–1888PubMedCrossRefGoogle Scholar
  36. 36.
    Colasanti J, Cho S-H, Wick S, Sundaresan V (1993) Localization of the functional p34cdc2 homolog of maize in root tip and stomatal complex cells: association with predicted division sites. Plant Cell 5:1101–1111PubMedCrossRefGoogle Scholar
  37. 37.
    Crowell EF, Bischoff V, Desprez T, Rolland A, Stierhof YD, Schumacher K, Gonneau M, Hofte H, Vernhettes S (2009) Pausing of Golgi bodies on microtubules regulates secretion of cellulose synthase complexes in Arabidopsis. Plant Cell 21:1141–1154PubMedCrossRefGoogle Scholar
  38. 38.
    De Schutter K, Joubes J, Cools T, Verkest A, Corellou F, Babiychuk E, Van Der Schueren E, Beeckman T, Kushnir S, Inze D, De Veylder L (2007) Arabidopsis WEE1 kinase controls cell cycle arrest in response to activation of the DNA integrity checkpoint. Plant Cell 19:211–225PubMedCrossRefGoogle Scholar
  39. 39.
    De Wulf P, Montani F, Visintin R (2009) Protein phosphatases take the mitotic stage. Curr Opin Cell Biol 21:806–815PubMedCrossRefGoogle Scholar
  40. 40.
    DeBolt S, Gutierrez R, Ehrhardt DW, Melo CV, Ross L, Cutler SR, Somerville C, Bonetta D (2007) Morlin, an inhibitor of cortical microtubule dynamics and cellulose synthase movement. Proc Natl Acad Sci USA 104:5854–5859PubMedCrossRefGoogle Scholar
  41. 41.
    Dewitte W, Murray JA (2003) The plant cell cycle. Annu Rev Plant Biol 54:235–264PubMedCrossRefGoogle Scholar
  42. 42.
    Dhonukshe P, Baluska F, Schlicht M, Hlavacka A, Samaj J, Friml J, Gadella TW Jr (2006) Endocytosis of cell surface material mediates cell plate formation during plant cytokinesis. Dev Cell 10:137–150PubMedCrossRefGoogle Scholar
  43. 43.
    Dhonukshe P, Laxalt AM, Goedhart J, Gadella TWJ, Munnik T (2003) Phospholipase D activation correlates with microtubule reorganization in living plant cells. Plant Cell 15:2666–2679PubMedCrossRefGoogle Scholar
  44. 44.
    Dhonukshe P, Mathur J, Hulskamp M, Gadella TW Jr (2005) Microtubule plus-ends reveal essential links between intracellular polarization and localized modulation of endocytosis during division-plane establishment in plant cells. BMC Biol 3:11PubMedCrossRefGoogle Scholar
  45. 45.
    Dissmeyer N, Nowack MK, Pusch S, Stals H, Inze D, Grini PE, Schnittger A (2007) T-loop phosphorylation of Arabidopsis CDKA;1 is required for its function and can be partially substituted by an aspartate residue. Plant Cell 19:972–985PubMedCrossRefGoogle Scholar
  46. 46.
    Dixit R, Chang E, Cyr R (2006) Establishment of polarity during organization of the acentrosomal plant cortical microtubule array. Mol Biol Cell 17:1298–1305PubMedCrossRefGoogle Scholar
  47. 47.
    Dixit R, Cyr R (2002) Golgi secretion is not required for marking the preprophase band site in cultured tobacco cells. Plant J 29:99–108PubMedCrossRefGoogle Scholar
  48. 48.
    Dixit R, Cyr R (2004) Encounters between dynamic cortical microtubules promote ordering of the cortical array through angle-dependent modifications of microtubule behavior. Plant Cell 16:3274–3284PubMedCrossRefGoogle Scholar
  49. 49.
    Dixit R, Cyr RJ (2002) Spatio-temporal relationship between nuclear-envelope breakdown and preprophase band disappearance in cultured tobacco cells. Protoplasma 219:116–121PubMedCrossRefGoogle Scholar
  50. 50.
    Doonan JH, Cove DJ, Corke FMK, Lloyd CW (1987) Pre-prophase band of microtubules, absent from tip-growing moss filaments, arises in leafy shoots during transition to intercalary growth. Cell Motil Cytoskeleton 7:138–153CrossRefGoogle Scholar
  51. 51.
    Dubois F, Bui Dang Ha D, Sangwan RS, Durand J (1996) The Petunia tra1 gene controls cell elongation and plant development, and mediates responses to cytokinins. Plant J 10:47–59CrossRefGoogle Scholar
  52. 52.
    Ehrhardt DW (2008) Straighten up and fly right: microtubule dynamics and organization of non-centrosomal arrays in higher plants. Curr Opin Cell Biol 20:107–116PubMedCrossRefGoogle Scholar
  53. 53.
    Eleftheriou EP, Palevitz BA (1992) The effect of cytochalasin D on preprophase band organization in root tip cells of Allium. J Cell Sci 103:989–998Google Scholar
  54. 54.
    Erhardt M, Stoppin-Mellet V, Campagne S, Canaday J, Mutterer J, Fabian T, Sauter M, Muller T, Peter C, Lambert AM, Schmit AC (2002) The plant Spc98p homologue colocalizes with gamma-tubulin at microtubule nucleation sites and is required for microtubule nucleation. J Cell Sci 115:2423–2431PubMedGoogle Scholar
  55. 55.
    Ferreira PC, Hemerly AS, Villarroel R, Van Montagu M, Inze D (1991) The Arabidopsis functional homolog of the p34cdc2 protein kinase. Plant Cell 3:531–540PubMedCrossRefGoogle Scholar
  56. 56.
    Flanders DJ, Rawlins DJ, Shaw PJ, Lloyd CW (1990) Nucleus-associated microtubules help determine the division plane of plant epidermal cells: avoidance of four-way junctions and the role of cell geometry. J Cell Biol 110:1111–1122PubMedCrossRefGoogle Scholar
  57. 57.
    Fulop K, Tarayre S, Kelemen Z, Horvath G, Kevei Z, Nikovics K, Bako L, Brown S, Kondorosi A, Kondorosi E (2005) Arabidopsis anaphase-promoting complexes – multiple activators and wide range of substrates might keep APC perpetually busy. Cell Cycle 4:1084–1092PubMedGoogle Scholar
  58. 58.
    Gaillard J, Neumann E, Van Damme D, Stoppin-Mellet V, Ebel C, Barbier E, Geelen D, Vantard M (2008) Two microtubule-associated proteins of Arabidopsis MAP65s promote antiparallel microtubule bundling. Mol Biol Cell 19:4534–4544PubMedCrossRefGoogle Scholar
  59. 59.
    Galatis B, Apostolakos P (2004) The role of the cytoskeleton in the morphogenesis and function of stomatal complexes. New Phytol 161:613–639CrossRefGoogle Scholar
  60. 60.
    Gallagher K, Smith LG (1999) Discordia mutations specifically misorient asymmetric cell divisions during development of the maize leaf epidermis. Development 126:4623–4633PubMedGoogle Scholar
  61. 61.
    Gardiner JC, Harper JD, 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 13:2143–2158PubMedCrossRefGoogle Scholar
  62. 62.
    Graham L (1996) Green algae to land plants: an evolutionary transition. J Plant Res 109:241–251CrossRefGoogle Scholar
  63. 63.
    Granger C, Cyr R (2001) Use of abnormal preprophase bands to decipher division plane determination. J Cell Sci 114:599–607PubMedGoogle Scholar
  64. 64.
    Gupton SL, Collings DA, Allen NS (2006) Endoplasmic reticulum targeted GFP reveals ER organization in tobacco NT-1 cells during cell division. Plant Physiol Biochem 44:95–105PubMedCrossRefGoogle Scholar
  65. 65.
    Gutierrez R, Lindeboom JJ, Paredez AR, Emons AM, Ehrhardt DW (2009) Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments. Nat Cell Biol 11:797–806PubMedCrossRefGoogle Scholar
  66. 66.
    Hamada T, Igarashi H, Itoh TJ, Shimmen T, Sonobe S (2004) Characterization of a 200 kDa microtubule-associated protein of tobacco BY-2 cells, a member of the XMAP215/MOR1 family. Plant Cell Physiol 45:1233–1242PubMedCrossRefGoogle Scholar
  67. 67.
    Hepler PK, Wolniak SM (1984) Membranes in the mitotic apparatus: their structure and function. Int Rev Cytol 90:169–238PubMedCrossRefGoogle Scholar
  68. 68.
    Hoshino H, Yoneda A, Kumagai F, Hasezawa S (2003) Roles of actin-depleted zone and preprophase band in determining the division site of higher-plant cells, a tobacco BY-2 cell line expressing GFP-tubulin. Protoplasma 222:157–165PubMedCrossRefGoogle Scholar
  69. 69.
    Hush J, Wu LP, John PCL, Hepler LH, Hepler PK (1996) Plant mitosis promoting factor disassembles the microtubule preprophase band and accelerates prophase progression in Tradescantia. Cell Biol Int 20:275–287PubMedCrossRefGoogle Scholar
  70. 70.
    Hush JM, Wadsworth P, Callaham DA, Hepler PK (1994) Quantification of microtubule dynamics in living plant-cells using fluorescence redistribution after photobleaching. J Cell Sci 107:775–784PubMedGoogle Scholar
  71. 71.
    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 50:915–924PubMedCrossRefGoogle Scholar
  72. 72.
    Inze D, De Veylder L (2006) Cell cycle regulation in plant development. Annu Rev Genet 40:77–105PubMedCrossRefGoogle Scholar
  73. 73.
    Iwakawa H, Shinmyo A, Sekine M (2006) Arabidopsis CDKA;1, a cdc2 homologue, controls proliferation of generative cells in male gametogenesis. Plant J 45:819–831PubMedCrossRefGoogle Scholar
  74. 74.
    Jackman M, Lindon C, Nigg EA, Pines J (2003) Active cyclin B1-Cdk1 first appears on centrosomes in prophase. Nat Cell Biol 5:143–148PubMedCrossRefGoogle Scholar
  75. 75.
    Jeganathan KB, Malureanu L, van Deursen JM (2005) The Rae1-Nup98 complex prevents aneuploidy by inhibiting securin degradation. Nature 438:1036–1039PubMedCrossRefGoogle Scholar
  76. 76.
    Jeong SY, Rose A, Joseph J, Dasso M, Meier I (2005) Plant-specific mitotic targeting of RanGAP requires a functional WPP domain. Plant J 42:270–282PubMedCrossRefGoogle Scholar
  77. 77.
    Joshi HC, Palevitz BA (1996) Gamma-tubulin and microtubule organization in plants. Trends Cell Biol 6:41–44PubMedCrossRefGoogle Scholar
  78. 78.
    Kaplan D (1992) The relationship of cells to organisms in plants: problem and implications of an organismal perspective. Int J Plant Sci 153:S28–S37CrossRefGoogle Scholar
  79. 79.
    Karahara I, Suda J, Staehelin LA, Mineyuki Y (2009) Technical note quantitative analysis of vesicles in the preprophase band by electron tomography. Cytologia 74:113–114Google Scholar
  80. 80.
    Katsuta J, Hashiguchi Y, Shibaoka H (1990) The role of the cytoskeleton in positioning of the nucleus in premitotic tobacco BY-2 Cells. J Cell Sci 95:413–422Google Scholar
  81. 81.
    Katsuta J, Shibaoka H (1988) The roles of the cytoskeleton and the cell wall in nuclear positioning in tabaccco BY-2 Cells. Plant Cell Physiol 29:403–413Google Scholar
  82. 82.
    Katsuta J, Shibaoka H (1992) Inhibition by kinase inhibitors of the development and the disappearance of the preprophase band of microtubules in tobacco BY-2 cells. J Cell Sci 103:397–405Google Scholar
  83. 83.
    Kawamura E, Himmelspach R, Rashbrooke MC, Whittington AT, Gale KR, Collings DA, Wasteneys GO (2006) MICROTUBULE ORGANIZATION 1 regulates structure and function of microtubule arrays during mitosis and cytokinesis in the Arabidopsis root. Plant Physiol 140:102–114PubMedCrossRefGoogle Scholar
  84. 84.
    Kawamura E, Wasteneys GO (2008) MOR1, the Arabidopsis thaliana homologue of Xenopus MAP215, promotes rapid growth and shrinkage, and suppresses the pausing of microtubules in vivo. J Cell Sci 121:4114–4123PubMedCrossRefGoogle Scholar
  85. 85.
    Ketelaar T, Faivre-Moskalenko C, Esseling JJ, de Ruijter NC, Grierson CS, Dogterom M, Emons AM (2002) Positioning of nuclei in Arabidopsis root hairs: an actin-regulated process of tip growth. Plant Cell 14:2941–2955PubMedCrossRefGoogle Scholar
  86. 86.
    Kirik V, Herrmann U, Parupalli C, Sedbrook JC, Ehrhardt DW, Hulskamp M (2007) CLASP localizes in two discrete patterns on cortical microtubules and is required for cell morphogenesis and cell division in Arabidopsis. J Cell Sci 120:4416–4425PubMedCrossRefGoogle Scholar
  87. 87.
    Korolev AV, Buschmann H, Doonan JH, Lloyd CW (2007) AtMAP70-5, a divergent member of the MAP70 family of microtubule-associated proteins, is required for anisotropic cell growth in Arabidopsis. J Cell Sci 120:2241–2247PubMedCrossRefGoogle Scholar
  88. 88.
    Korolev AV, Chan J, Naldrett MJ, Doonan JH, Lloyd CW (2005) Identification of a novel family of 70 kDa microtubule-associated proteins in Arabidopsis cells. Plant J 42:547–555PubMedCrossRefGoogle Scholar
  89. 89.
    Krupnova T, Sasabe M, Ghebreghiorghis L, Gruber CW, Hamada T, Dehmel V, Strompen G, Stierhof YD, Lukowitz W, Kemmerling B, Machida Y, Hashimoto T, Mayer U, Jurgens G (2009) Microtubule-associated kinase-like protein RUNKEL needed for cell plate expansion in Arabidopsis cytokinesis. Curr Biol 19:518–523PubMedCrossRefGoogle Scholar
  90. 90.
    Kutsuna N, Hasezawa S (2002) Dynamic organization of vacuolar and microtubule structures during cell cycle progression in synchronized tobacco BY-2 cells. Plant Cell Physiol 43:965–973PubMedCrossRefGoogle Scholar
  91. 91.
    Kutsuna N, Kumagai F, Sato MH, Hasezawa S (2003) Three-dimensional reconstruction of tubular structure of vacuolar membrane throughout mitosis in living tobacco cells. Plant Cell Physiol 44:1045–1054PubMedCrossRefGoogle Scholar
  92. 92.
    Lee J, Das A, Yamaguchi M, Hashimoto J, Tsutsumi N, Uchimiya H, Umeda M (2003) Cell cycle function of a rice B2-type cyclin interacting with a B-type cyclin-dependent kinase. Plant J 34:417–425PubMedCrossRefGoogle Scholar
  93. 93.
    Lee JY, Lee HS, Wi SJ, Park KY, Schmit AC, Pai HS (2009) Dual functions of Nicotiana benthamiana Rae1 in interphase and mitosis. Plant J 59:278–291PubMedCrossRefGoogle Scholar
  94. 94.
    Li H, Zeng X, Liu ZQ, Meng QT, Yuan M, Mao TL (2009) Arabidopsis microtubule-associated protein AtMAP65-2 acts as a microtubule stabilizer. Plant Mol Biol 69:313–324PubMedCrossRefGoogle Scholar
  95. 95.
    Liu B, Joshi HC, Wilson TJ, Silflow CD, Palevitz BA, Snustad DP (1994) Gamma-tubulin in Arabidopsis: gene sequence, immunoblot, and immunofluorescence studies. Plant Cell 6:303–314PubMedCrossRefGoogle Scholar
  96. 96.
    Liu B, Marc J, Joshi HC, Palevitz BA (1993) A gamma-tubulin-related protein associated with the microtubule arrays of higher plants in a cell cycle-dependent manner. J Cell Sci 104:1217–1228PubMedGoogle Scholar
  97. 97.
    Lloyd C (1991) Cytoskeletal elements of the phragmosome establish the division plane in vacuolated higher plant cells. In: Lloyd C (ed) The cytoskeletal basis of plant growth and form. Academic, London, pp 245–257Google Scholar
  98. 98.
    Lunn JE (2007) Compartmentation in plant metabolism. J Exp Bot 58:35–47PubMedCrossRefGoogle Scholar
  99. 99.
    Mao G, Chan J, Calder G, Doonan JH, Lloyd CW (2005) Modulated targeting of GFP-AtMAP65-1 to central spindle microtubules during division. Plant J 43:469–478PubMedCrossRefGoogle Scholar
  100. 100.
    Mao T, Jin L, Li H, Liu B, Yuan M (2005) Two microtubule-associated proteins of the Arabidopsis MAP65 family function differently on microtubules. Plant Physiol 138:654–662PubMedCrossRefGoogle Scholar
  101. 101.
    Marcus AI, Ambrose JC, Blickley L, Hancock WO, Cyr RJ (2002) Arabidopsis thaliana protein, ATK1, is a minus-end directed kinesin that exhibits non-processive movement. Cell Motil Cytoskeleton 52:144–150PubMedCrossRefGoogle Scholar
  102. 102.
    Marcus AI, Dixit R, Cyr RJ (2005) Narrowing of the preprophase microtubule band is not required for cell division plane determination in cultured plant cells. Protoplasma 226:169–174PubMedCrossRefGoogle Scholar
  103. 103.
    Marcus AI, Li W, Ma H, Cyr RJ (2003) A kinesin mutant with an atypical bipolar spindle undergoes normal mitosis. Mol Biol Cell 14:1717–1726PubMedCrossRefGoogle Scholar
  104. 104.
    Marty F (1999) Plant vacuoles. Plant Cell 11:587–600PubMedCrossRefGoogle Scholar
  105. 105.
    Mathur J, Mathur N, Kernebeck B, Srinivas BP, Hulskamp M (2003) A novel localization pattern for an EB1-like protein links microtubule dynamics to endomembrane organization. Curr Biol 13:1991–1997PubMedCrossRefGoogle Scholar
  106. 106.
    Mayer Y, Torres Ruiz RA, Berleth T, Misera S, Jurgens G (1991) Mutations affecting body organization in the Arabidopsis embryo. Nature 353:402–407CrossRefGoogle Scholar
  107. 107.
    McClinton RS, Sung ZR (1997) Organization of cortical microtubules at the plasma membrane in Arabidopsis. Planta 201:252–260PubMedCrossRefGoogle Scholar
  108. 108.
    Meszaros T, Miskolczi P, Ayaydin F, Pettko-Szandtner A, Peres A, Magyar Z, Horvath GV, Bako L, Feher A, Dudits D (2000) Multiple cyclin-dependent kinase complexes and phosphatases control G2/M progression in alfalfa cells. Plant Mol Biol 43:595–605PubMedCrossRefGoogle Scholar
  109. 109.
    Mews M, Sek FJ, Moore R, Volkmann D, Gunning BES, John PCL (1997) Mitotic cyclin distribution during maize cell division: implications for the sequence diversity and function of cyclins in plants. Protoplasma 200:128–145CrossRefGoogle Scholar
  110. 110.
    Mineyuki Y (1999) The preprophase band of microtubules: its function as a cytokinetic apparatus in higher plants. Int Rev Cytol 187:1–49CrossRefGoogle Scholar
  111. 111.
    Mineyuki Y, Aioi H, Yamashita M, Nagahama Y (1996) A comparative study on stainability of preprophase bands by the PSTAIR antibody. J Plant Res 109:185–192CrossRefGoogle Scholar
  112. 112.
    Mineyuki Y, Palevitz BA (1990) Relationship between preprophase band organization, F-actin and the division site in Allium. J Cell Sci 97:283–295Google Scholar
  113. 113.
    Mineyuki Y, Yamashita M, Nagahama Y (1991) P34cdc2 kinase homolog in the preprophase band. Protoplasma 162:182–186CrossRefGoogle Scholar
  114. 114.
    Muller J, Beck M, Mettbach U, Komis G, Hause G, Menzel D, Samaj J (2010) Arabidopsis MPK6 is involved in cell division plane control during early root development, and localizes to the pre-prophase band, phragmoplast, trans-Golgi network and plasma membrane. Plant J 61:234–248PubMedCrossRefGoogle Scholar
  115. 115.
    Muller S, Han SC, Smith LG (2006) Two kinesins are involved in the spatial control of cytokinesis in Arabidopsis thaliana. Curr Biol 16:888–894PubMedCrossRefGoogle Scholar
  116. 116.
    Muller S, Smertenko A, Wagner V, Heinrich M, Hussey PJ, Hauser MT (2004) The plant microtubule-associated protein AtMAP65-3/PLE is essential for cytokinetic phragmoplast function. Curr Biol 14:412–417PubMedCrossRefGoogle Scholar
  117. 117.
    Murata T, Sonobe S, Baskin TI, Hyodo S, Hasezawa S, Nagata T, Horio T, Hasebe M (2005) Microtubule-dependent microtubule nucleation based on recruitment of gamma-tubulin in higher plants. Nat Cell Biol 7:961–968PubMedCrossRefGoogle Scholar
  118. 118.
    Murata T, Wada M (1991) Effects of centrifugation on preprophase band formation in Adiantum protonemata. Planta 183:391–398CrossRefGoogle Scholar
  119. 119.
    Nakajima K, Furutani I, Tachimoto H, Matsubara H, Hashimoto T (2004) SPIRAL1 encodes a plant-specific microtubule-localized protein required for directional control of rapidly expanding Arabidopsis cells. Plant Cell 16:1178–1190PubMedCrossRefGoogle Scholar
  120. 120.
    Nebenfuhr A, Frohlick JA, Staehelin LA (2000) Redistribution of golgi stacks and other organelles during mitosis and cytokinesis in plant cells. Plant Physiol 124:135–151PubMedCrossRefGoogle Scholar
  121. 121.
    Niethammer P, Kronja I, Kandels-Lewis S, Rybina S, Bastiaens P, Karsenti E (2007) Discrete states of a protein interaction network govern interphase and mitotic microtubule dynamics. PLoS Biol 5:e29PubMedCrossRefGoogle Scholar
  122. 122.
    Nogami A, Mineyuki Y (1999) Loosening of a preprophase band of microtubules in onion (Allium cepa L.) root tip cells by kinase inhibitors. Cell Struct Funct 24:419–424PubMedCrossRefGoogle Scholar
  123. 123.
    Nogami A, Suzaki T, Shigenaka Y, Nagahama Y, Mineyuki Y (1996) Effects of cycloheximide on preprophase bands and prophase spindles in onion (Allium cepa L) root tip cells. Protoplasma 192:109–121CrossRefGoogle Scholar
  124. 124.
    Nowack MK, Grini PE, Jakoby MJ, Lafos M, Koncz C, Schnittger A (2006) A positive signal from the fertilization of the egg cell sets off endosperm proliferation in angiosperm embryogenesis. Nat Genet 38:63–67PubMedCrossRefGoogle Scholar
  125. 125.
    O’Farrell PH (2001) Triggering the all-or-nothing switch into mitosis. Trends Cell Biol 11:512–519PubMedCrossRefGoogle Scholar
  126. 126.
    Palevitz BA (1987) Actin in the preprophase band of Allium cepa. J Cell Biol 104:1515–1519PubMedCrossRefGoogle Scholar
  127. 127.
    Panteris E (2008) Cortical actin filaments at the division site of mitotic plant cells: a reconsideration of the “actin-depleted zone”. New Phytol 179:334–341PubMedCrossRefGoogle Scholar
  128. 128.
    Panteris E, Apostolakos P, Galatis B (1995) The effect of taxol on triticum preprophase root cells: preprophase microtubule band organization seems to depend on new microtubule assembly. Protoplasma 186:72–78CrossRefGoogle Scholar
  129. 129.
    Panteris E, Apostolakos P, Galatis B (2006) Cytoskeletal asymmetry in Zea mays subsidiary cell mother cells: a monopolar prophase microtubule half-spindle anchors the nucleus to its polar position. Cell Motil Cytoskeleton 63:696–709PubMedCrossRefGoogle Scholar
  130. 130.
    Panteris E, Apostolakos P, Quader H, Galatis B (2004) A cortical cytoplasmic ring predicts the division plane in vacuolated cells of Coleus: the role of actomyosin and microtubules in the establishment and function of the division site. New Phytol 163:271–286CrossRefGoogle Scholar
  131. 131.
    Papaseit C, Pochon N, Tabony J (2000) Microtubule self-organization is gravity-dependent. Proc Natl Acad Sci USA 97:8364–8368PubMedCrossRefGoogle Scholar
  132. 132.
    Paradez A, Wright A, Ehrhardt DW (2006) Microtubule cortical array organization and plant cell morphogenesis. Curr Opin Plant Biol 9:571–578PubMedCrossRefGoogle Scholar
  133. 133.
    Pastuglia M, Bouchez D (2007) Molecular encounters at microtubule ends in the plant cell cortex. Curr Opin Plant Biol 10:557–563PubMedCrossRefGoogle Scholar
  134. 134.
    Pickett-Heaps JD, Gunning BES, Brown RC, Lemmon BE, Cleary AL (1999) The cytoplast concept in dividing plant cells: cytoplasmic domains and the evolution of spatially organized cell division. Am J Bot 86:153–172CrossRefGoogle Scholar
  135. 135.
    Pickett-Heaps JD, Northcote DH (1966) Organization of microtubules and endoplasmic reticulum during mitosis and cytokinesis in wheat meristems. J Cell Sci 1:109–120PubMedGoogle Scholar
  136. 136.
    Preuss ML, Delmer DP, Liu B (2003) The cotton kinesin-like calmodulin-binding protein associates with cortical microtubules in cotton fibers. Plant Physiol 132:154–160PubMedCrossRefGoogle Scholar
  137. 137.
    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 44:595–605PubMedCrossRefGoogle Scholar
  138. 138.
    Sasabe M, Soyano T, Takahashi Y, Sonobe S, Igarashi H, Itoh TJ, Hidaka M, Machida Y (2006) Phosphorylation of NtMAP65-1 by a MAP kinase down-regulates its activity of microtubule bundling and stimulates progression of cytokinesis of tobacco cells. Genes Dev 20:1004–1014PubMedCrossRefGoogle Scholar
  139. 139.
    Schlaitz AL, Srayko M, Dammermann A, Quintin S, Wielsch N, MacLeod I, de Robillard Q, Zinke A, Yates JR 3rd, Muller-Reichert T, Shevchenko A, Oegema K, Hyman AA (2007) The C. elegans RSA complex localizes protein phosphatase 2A to centrosomes and regulates mitotic spindle assembly. Cell 128:115–127PubMedCrossRefGoogle Scholar
  140. 140.
    Sedbrook JC, Ehrhardt DW, Fisher SE, Scheible WR, Somerville CR (2004) The Arabidopsis SKU6/SPIRAL1 gene encodes a plus end-localized microtubule-interacting protein involved in directional cell expansion. Plant Cell 16:1506–1520PubMedCrossRefGoogle Scholar
  141. 141.
    Segui-Simarro JM, Staehelin LA (2006) Cell cycle-dependent changes in Golgi stacks, vacuoles, clathrin-coated vesicles and multivesicular bodies in meristematic cells of Arabidopsis thaliana: a quantitative and spatial analysis. Planta 223:223–236PubMedCrossRefGoogle Scholar
  142. 142.
    Shaw SL, Kamyar R, Ehrhardt DW (2003) Sustained microtubule treadmilling in Arabidopsis cortical arrays. Science 300:1715–1718PubMedCrossRefGoogle Scholar
  143. 143.
    Shoji T, Narita NN, Hayashi K, Asada J, Hamada T, Sonobe S, Nakajima K, Hashimoto T (2004) Plant-specific microtubule-associated protein SPIRAL2 is required for anisotropic growth in arabidopsis. Plant Physiol 136:3933–3944PubMedCrossRefGoogle Scholar
  144. 144.
    Sinnott EW, Bloch R (1940) Cytoplasmic behavior during division of vacuolate plant cells. Proc Natl Acad Sci USA 26:223–227PubMedCrossRefGoogle Scholar
  145. 145.
    Slep KC (2009) The role of TOG domains in microtubule plus end dynamics. Biochem Soc Trans 37:1002–1006PubMedCrossRefGoogle Scholar
  146. 146.
    Smertenko AP, Chang HY, Sonobe S, Fenyk SI, Weingartner M, Bogre L, Hussey PJ (2006) Control of the AtMAP65-1 interaction with microtubules through the cell cycle. J Cell Sci 119:3227–3237PubMedCrossRefGoogle Scholar
  147. 147.
    Smertenko AP, Chang HY, Wagner V, Kaloriti D, Fenyk S, Sonobe S, Lloyd C, Hauser MT, Hussey PJ (2004) The Arabidopsis microtubule-associated protein AtMAP65-1: molecular analysis of its microtubule bundling activity. Plant Cell 16:2035–2047PubMedCrossRefGoogle Scholar
  148. 148.
    Smith LG, Gerttula SM, Han SC, Levy J (2001) TANGLED1: a microtubule binding protein required for the spatial control of cytokinesis in maize. J Cell Biol 152:231–236PubMedCrossRefGoogle Scholar
  149. 149.
    Smith LG, Hake S, Sylvester AW (1996) The tangled-1 mutation alters cell division orientations throughout maize leaf development without altering leaf shape. Development 122:481–489PubMedGoogle Scholar
  150. 150.
    Spinner L, Pastuglia M, Belcram K, Pegoraro M, Goussot M, Bouchez D, Schaefer D (2010) The function of TONNEAU1 in moss reveals ancient mechanisms of division plane specification and cell elongation in land plants. Development 137:2733–2742PubMedCrossRefGoogle Scholar
  151. 151.
    Stals H, Bauwens S, Traas J, Van Montagu M, Engler G, Inze D (1997) Plant CDC2 is not only targeted to the pre-prophase band, but also co-localizes with the spindle, phragmoplast, and chromosomes. FEBS Lett 418:229–234PubMedCrossRefGoogle Scholar
  152. 152.
    Stoppin V, Vantard M, Schmit AC, Lambert AM (1994) Isolated plant nuclei nucleate microtubule assembly: the nuclear surface in higher plants has centrosome-like activity. Plant Cell 6:1099–1106PubMedCrossRefGoogle Scholar
  153. 153.
    Takatsuka H, Ohno R, Umeda M (2009) The Arabidopsis cyclin-dependent kinase-activating kinase CDKF;1 is a major regulator of cell proliferation and cell expansion but is dispensable for CDKA activation. Plant J 59:475–487PubMedCrossRefGoogle Scholar
  154. 154.
    Torres-Ruiz RA, Jürgens G (1994) Mutations in the Fass gene uncouple pattern formation and morphogenesis in Arabidopsis development. Development 120:2967–2978PubMedGoogle Scholar
  155. 155.
    Traas J, Bellini C, Nacry P, Kronenberger J, Bouchez D, Caboche M (1995) Normal differentiation patterns in plants lacking microtubular preprophase bands. Nature 375:676–677CrossRefGoogle Scholar
  156. 156.
    Traas JA, Doonan JD, 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 105:387–395PubMedCrossRefGoogle Scholar
  157. 157.
    Twell D, Park SK, Hawkins TJ, Schubert D, Schmidt R, Smertenko A, Hussey PJ (2002) MOR1/GEM1 has an essential role in the plant-specific cytokinetic phragmoplast. Nat Cell Biol 4:711–714PubMedCrossRefGoogle Scholar
  158. 158.
    Umeda M, Shimotohno A, Yamaguchi M (2005) Control of cell division and transcription by cyclin-dependent kinase-activating kinases in plants. Plant Cell Physiol 46:1437–1442PubMedCrossRefGoogle Scholar
  159. 159.
    Van Damme D (2009) Division plane determination during plant somatic cytokinesis. Curr Opin Plant Biol 12:745–751PubMedCrossRefGoogle Scholar
  160. 160.
    Van Damme D, Bouget FY, Van Poucke K, Inze D, Geelen D (2004) Molecular dissection of plant cytokinesis and phragmoplast structure: a survey of GFP-tagged proteins. Plant J 40:386–398PubMedCrossRefGoogle Scholar
  161. 161.
    Van Damme D, Vanstraelen M, Geelen D (2007) Cortical division zone establishment in plant cells. Trends Plant Sci 12:458–464PubMedCrossRefGoogle Scholar
  162. 162.
    van der Vaart B, Akhmanova A, Straube A (2009) Regulation of microtubule dynamic instability. Biochem Soc Trans 37:1007–1013PubMedCrossRefGoogle Scholar
  163. 163.
    Van Leene J, Stals H, Eeckhout D, Persiau G, Van Slijke E, Van Isterdael G, De Clercq A, Bonnet E, Laukens K, Remmerie N, Hendrickx K, De Vijlder T, Adbelkrim A, Pharazyn A, Van Onckelen H, Inze D, Witters E, De Jaeger G (2007) A tandem affinity purification-based technology platform to study the cell cycle interactome in Arabidopsis thaliana. Mol Cell Proteomics 6:1226–1238PubMedCrossRefGoogle Scholar
  164. 164.
    Vanstraelen M, Van Damme D, De Rycke R, Mylle E, Inze D, Geelen D (2006) Cell cycle-dependent targeting of a kinesin at the plasma membrane demarcates the division site in plant cells. Curr Biol 16:308–314PubMedCrossRefGoogle Scholar
  165. 165.
    Venverloo CJ, Libbenga KR (1987) Regulation of the plane of cell division in vacuolated cells. I. The function of nuclear positioning and phragmosome formation. J Plant Physiol 131:267–284Google Scholar
  166. 166.
    Vos JW, Dogterom M, Emons AM (2004) Microtubules become more dynamic but not shorter during preprophase band formation: a possible “search-and-capture” mechanism for microtubule translocation. Cell Motil Cytoskeleton 57:246–258PubMedCrossRefGoogle Scholar
  167. 167.
    Walia A, Lee JS, Wasteneys G, Ellis B (2009) Arabidopsis mitogen-activated protein kinase MPK18 mediates cortical microtubule functions in plant cells. Plant J 59:565–575PubMedCrossRefGoogle Scholar
  168. 168.
    Walker KL, Muller S, Moss D, Ehrhardt DW, Smith LG (2007) Arabidopsis TANGLED identifies the division plane throughout mitosis and cytokinesis. Curr Biol 17:1827–1836PubMedCrossRefGoogle Scholar
  169. 169.
    Wang H, Cutler AJ, Fowke LC (1991) DNA-replication and the development of preprophase bands in soybean protoplast cultures. Physiol Plant 82:150–156CrossRefGoogle Scholar
  170. 170.
    Wang H, Fowke LC, Crosby WL (1997) A plant cyclin-dependent kinase inhibitor gene. Nature 386:451–452PubMedCrossRefGoogle Scholar
  171. 171.
    Wang H, Zhou Y, Bird DA, Fowke LC (2008) Functions, regulation and cellular localization of plant cyclin-dependent kinase inhibitors. J Microsc 231:234–246PubMedCrossRefGoogle Scholar
  172. 172.
    Weingartner M, Binarova P, Drykova D, Schweighofer A, David JP, Heberle-Bors E, Doonan J, Bogre L (2001) Dynamic recruitment of Cdc2 to specific microtubule structures during mitosis. Plant Cell 13:1929–1943PubMedCrossRefGoogle Scholar
  173. 173.
    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 411:610–613PubMedCrossRefGoogle Scholar
  174. 174.
    Wick SM (1991) Spatial aspects of cytokinesis in plant cells. Curr Opin Cell Biol 3:253–260PubMedCrossRefGoogle Scholar
  175. 175.
    Wick SM, Duniec J (1983) Immunofluorescence microscopy of tubulin and microtubule arrays in plant cells. II. Transition between the pre-prophase band and the mitotic. Protoplasma 122:45–55CrossRefGoogle Scholar
  176. 176.
    Wightman R, Turner SR (2007) Severing at sites of microtubule crossover contributes to microtubule alignment in cortical arrays. Plant J 52:742–751PubMedCrossRefGoogle Scholar
  177. 177.
    Wilde A, Lizarraga SB, Zhang L, Wiese C, Gliksman NR, Walczak CE, Zheng Y (2001) Ran stimulates spindle assembly by altering microtubule dynamics and the balance of motor activities. Nat Cell Biol 3:221–227PubMedCrossRefGoogle Scholar
  178. 178.
    Wright AJ, Gallagher K, Smith LG (2009) discordia1 and alternative discordia1 function redundantly at the cortical division site to promote preprophase band formation and orient division planes in maize. Plant Cell 21:234–247PubMedCrossRefGoogle Scholar
  179. 179.
    Wright AJ, Smith LG (2008) Division plane orientation in plant cells. In: Verma DPS, Hong Z (eds) Plant cell monographs, vol. 9 cell division control in plants. Springer, Berlin, pp 33–57CrossRefGoogle Scholar
  180. 180.
    Xu XFM, Zhao Q, Rodrigo-Peiris T, Brkljacic J, He CS, Muller S, Meier I (2008) RanGAP1 is a continuous marker of the Arabidopsis cell division plane. Proc Natl Acad Sci USA 105:18637–18642PubMedCrossRefGoogle Scholar
  181. 181.
    Yanagawa Y, Hasezawa S, Kumagai F, Oka M, Fujimuro M, Naito T, Makino T, Yokosawa H, Tanaka K, Komamine A, Hashimoto J, Sato T, Nakagawa H (2002) Cell-cycle dependent dynamic change of 26S proteasome distribution in tobacco BY-2 cells. Plant Cell Physiol 43:604–613PubMedCrossRefGoogle Scholar
  182. 182.
    Yao M, Wakamatsu Y, Itoh TJ, Shoji T, Hashimoto T (2008) Arabidopsis SPIRAL2 promotes uninterrupted microtubule growth by suppressing the pause state of microtubule dynamics. J Cell Sci 121:2372–2381PubMedCrossRefGoogle Scholar
  183. 183.
    Zachariadis M, Quader H, Galatis B, Apostolakos P (2001) Endoplasmic reticulum preprophase band in dividing root-tip cells of Pinus brutia. Planta 213:824–827PubMedCrossRefGoogle Scholar
  184. 184.
    Zhou Y, Fowke LC, Wang H (2002) Plant CDK inhibitors: studies of interactions with cell cycle regulators in the yeast two-hybrid system and functional comparisons in transgenic Arabidopsis plants. Plant Cell Reports 20:967–975CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  1. 1.Station de Génétique et Amélioration des Plantes, INRA Centre de VersaillesInstitut Jean-Pierre BourginVersailles, CedexFrance

Personalised recommendations