Microtubule networks for plant cell division

Systems and Synthetic Biology

Volumn 8, Issue 3, 2014, Pages 187-194

  de Keijzer, Jeroen ^a   Mulder, Bela M ^a,b   Janson, Marcel E ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b FOM INSTITUTE AMOLF   (Netherlands)

Author keywords

Cortical array; Cytokinesis; Cytoskeleton; Microtubule; Phragmoplast; Plant

Indexed keywords

EID: 84897118241     PISSN: 18725325     EISSN: 18725333     Source Type: Journal    
DOI: 10.1007/s11693-014-9142-x     Document Type: Review

References (98)

1. Al-Bassam J, Kim H, Brouhard G et al (2010) CLASP promotes microtubule rescue by recruiting tubulin dimers to the microtubule. Dev Cell 19:245–258. doi:10.1016/j.devcel.2010.07.016
2. Allard JF, Ambrose JC, Wasteneys GO, Cytrynbaum EN (2010a) A mechanochemical model explains interactions between cortical microtubules in plants. Biophys J 99:1082–1090. doi:10.1016/j.bpj.2010.05.037
3. Allard JF, Wasteneys GO, Cytrynbaum EN (2010b) Mechanisms of self-organization of cortical microtubules in plants revealed by computational simulations. Mol Biol Cell 21:278–286
4. Ambrose C, Wasteneys GO (2012) Nanoscale and geometric influences on the microtubule cytoskeleton in plants: thinking inside and outside the box. Protoplasma 249(Suppl):S69–S76. doi:10.1007/s00709-011-0334-x
5. Ambrose C, Allard JF, Cytrynbaum EN, Wasteneys GO (2011) A CLASP-modulated cell edge barrier mechanism drives cell-wide cortical microtubule organization in Arabidopsis. Nat Commun 2:430. doi:10.1038/ncomms1444
6. Asada T, Sonobe S, Shibaoka H (1991) Microtubule translocation in the cytokinetic apparatus of cultured tobacco cells. Nature 350:238–241
7. Bieling P, Telley I, Surrey T (2010) A minimal midzone protein module controls formation and length of antiparallel microtubule overlaps. Cell 142:420–432. doi:10.1016/j.cell.2010.06.033
8. Bratman SV, Chang F (2007) Stabilization of overlapping microtubules by fission yeast CLASP. Dev Cell 13:812–827. doi:10.1016/j.devcel.2007.10.015
9. Braun M, Lansky Z, Fink G et al (2011) Adaptive braking by Ase1 prevents overlapping microtubules from sliding completely apart. Nat Cell Biol 13:1259–1264. doi:10.1038/ncb2323
10. Chan J, Sambade A, Calder G, Lloyd C (2009) Arabidopsis cortical microtubules are initiated along, as well as branching from, existing microtubules. Plant Cell 12:2298–2306
11. Clausen T, Ribbeck K (2007) Self-organization of anastral spindles by synergy of dynamic instability, autocatalytic microtubule production, and a spatial signaling gradient. PLoS ONE 2:e244. doi:10.1371/journal.pone.0000244
12. 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 10:1875–1888
13. 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 103:977–988
14. De Mey J, Lambert AM, Bajer AS et al (1982) Visualization of microtubules in interphase and mitotic plant cells of Haemanthus endosperm with the immuno-gold staining method. Proc Natl Acad Sci U S A 79:1898–1902
15. De Storme N, Geelen D (2013) Cytokinesis in plant male meiosis. Plant Signal Behav 8:e23394. doi:10.4161/psb.23394
16. Deinum EE (2013) Simple models for complex questions on plant development (Chapter 9). Dissertion, Wageningen University
17. Deinum EE, Mulder BM (2013) Modelling the role of microtubules in plant cell morphology. Curr Opin Plant Biol 16:688–692
18. Dhonukshe P, Vischer N, Gadella TWJ (2006) Contribution of microtubule growth polarity and flux to spindle assembly and functioning in plant cells. J Cell Sci 119:3193–3205. doi:10.1242/jcs.03048
19. 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 16:3274–3284. doi:10.1105/tpc.104.026930
20. Ehrhardt DW, Shaw SL (2006) Microtubule dynamics and organization in the plant cortical array. Annu Rev Plant Biol 57:859–875
21. Eren EC, Dixit R, Gautam N (2010) A 3D computer simulation model reveals the mechanisms for self-organization of plant cortical microtubules into oblique arrays. Mol Biol Cell 21:2674–2684
22. Euteneuer U, Mcintosh JR (1980) Polarity of midbody and phragmoplast microtubules. J Cell Biol 87:509–515
23. Fu C, Ward JJ, Loiodice I et al (2009) Phospho-regulated interaction between kinesin-6 Klp9p and microtubule bundler Ase1p promotes spindle elongation. Dev Cell 17:257–267. doi:10.1016/j.devcel.2009.06.012
24. Fuller BG, Lampson M, Foley E et al (2008) Midzone activation of aurora B in anaphase produces an intracellular phosphorylation gradient. Nature 453:1132–1136. doi:10.1038/nature06923
25. Gallagher K, Smith LG (1999) Discordia mutations specifically misorient asymmetric cell divisions during development of the maize leaf epidermis. Development 126:4623–4633
26. Gardner MK, Zanic M, Howard J (2013) Microtubule catastrophe and rescue. Curr Opin Cell Biol 25:14–22. doi:10.1016/j.ceb.2012.09.006
27. Glotzer M (2009) The 3Ms of central spindle assembly: microtubules, motors and MAPs. Nat Rev Mol Cell Biol 10:9–20. doi:10.1038/nrm2609
28. Hawkins R, Tindemans S, Mulder B (2010) Model for the orientational ordering of the plant microtubule cortical array. Phys Rev E. doi:10.1103/PhysRevE.82.011911
29. Hiwatashi Y, Obara M, Sato Y et al (2008) Kinesins are indispensable for interdigitation of phragmoplast microtubules in the moss Physcomitrella patens. Plant Cell 20:3094–3106. doi:10.1105/tpc.108.061705
30. Ho C-MK, Hotta T, Guo F et al (2011a) Interaction of antiparallel microtubules in the phragmoplast is mediated by the microtubule-associated protein MAP65-3 in Arabidopsis. Plant Cell 23:2909–2923. doi:10.1105/tpc.110.078204
31. Ho C-MK, Hotta T, Kong Z et al (2011b) Augmin plays a critical role in organizing the spindle and phragmoplast microtubule arrays in Arabidopsis. Plant Cell 23:2606–2618. doi:10.1105/tpc.111.086892
32. Hotta T, Kong Z, Ho C-MK et al (2012) Characterization of the Arabidopsis augmin complex uncovers its critical function in the assembly of the acentrosomal spindle and phragmoplast microtubule arrays. Plant Cell 24:1494–1509. doi:10.1105/tpc.112.096610
33. Hu C-K, Coughlin M, Field CM, Mitchison TJ (2011) KIF4 regulates midzone length during cytokinesis. Curr Biol 21:815–824. doi:10.1016/j.cub.2011.04.019
34. Ishizaki K, Johzuka-Hisatomi Y, Ishida S et al (2013) Homologous recombination-mediated gene targeting in the liverwort Marchantia polymorpha L. Sci Rep 3:1532
35. Janson ME, Loughlin R, Loïodice I et al (2007) Crosslinkers and motors organize dynamic microtubules to form stable bipolar arrays in fission yeast. Cell 128:357–368. doi:10.1016/j.cell.2006.12.030
36. Jensen C, Bajer A (1973) Spindle dynamics and arrangement of microtubules. Chromosoma 44:73–89. doi:10.1007/BF00372574
37. Kamasaki T, O’Toole E, Kita S et al (2013) Augmin-dependent microtubule nucleation at microtubule walls in the spindle. J Cell Biol 202:25–33
38. Kapitein LC, Peterman EJG, Kwok BH et al (2005) The bipolar mitotic kinesin Eg5 moves on both microtubules that it crosslinks. Nature 435:114–118
39. Kosetsu K, de Keijzer J, Janson ME, Goshima G (2013) MICROTUBULE-ASSOCIATED PROTEIN65 is essential for maintenance of phragmoplast bipolarity and formation of the cell plate in Physcomitrella patens. Plant Cell 1–15. doi:10.1105/tpc.113.117432
40. Lee YR, Liu B (2000) Identification of a phragmoplast-associated kinesin-related protein in higher plants. Curr Biol 10:797–800
41. Lee Y-RJ, Liu B (2013) The rise and fall of the phragmoplast microtubule array. Curr Opin Plant Biol 16:757–763. doi:10.1016/j.pbi.2013.10.008
42. Lee YJ, Giang HM, Liu B (2001) A novel plant kinesin-related protein specifically associates with the phragmoplast organelles. Plant Cell 13:2427–2439. doi:10.1105/tpc.010225.because
43. Lee Y-RJ, Li Y, Liu B (2007) Two Arabidopsis phragmoplast-associated kinesins play a critical role in cytokinesis during male gametogenesis. Plant Cell 19:2595–2605. doi:10.1105/tpc.107.050716
44. Lindeboom JJ, Nakamura M, Hibbel A et al (2013) A mechanism for reorientation of cortical microtubule arrays driven by microtubule severing. Science 342(6163):1245533
45. 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(Pt 4):1217–1228
46. Liu J, Wang Z, Jiang K et al (2009) PRC1 cooperates with CLASP1 to organize central spindle plasticity in mitosis. J Biol Chem 284:23059–23071. doi:10.1074/jbc.M109.009670
47. Lloyd CW, Traas JA (1988) The role of F-actin in determining the division plane of carrot suspension cells. Drug studies. Development 102:211–221
48. Maizel A, von Wangenheim D, Federici F et al (2011) High-resolution live imaging of plant growth in near physiological bright conditions using light sheet fluorescence microscopy. Plant J 68:377–385
49. Masoud K, Herzog E, Chabouté M-E, Schmit A-C (2013) Microtubule nucleation and establishment of the mitotic spindle in vascular plant cells. Plant J 75:245–257. doi:10.1111/tpj.12179
50. Mcmichael CM, Bednarek SY (2013) Cytoskeletal and membrane dynamics during higher plant cytokinesis. New Phytol 197:1039–1057
51. Miki T, Naito H, Nishina M, Goshima G (2014) Endogenous localizome identifies 43 mitotic kinesins in a plant cell. Proc Natl Acad Sci U S A 111(11):E1053–E1061
52. Mineyuki Y, Gunning BES (1990) A role for preprophase bands of microtubules in maturation of new cell walls, and a general proposal on the function of preprophase band sites in cell division in higher plants. J Cell Sci 97:527–537
53. Müller S, Smertenko A, Wagner V et al (2004) The plant microtubule-associated protein AtMAP65-3/PLE is essential for cytokinetic phragmoplast function. Curr Biol 14:412–417. doi:10.1016/j.cub.2004.02.032
54. Müller S, Han S, Smith LG (2006) Two kinesins are involved in the spatial control of cytokinesis in Arabidopsis thaliana. Curr Biol 16:888–894. doi:10.1016/j.cub.2006.03.034
55. Müller S, Wright AJ, Smith LG (2009) Division plane control in plants: new players in the band. Trends Cell Biol 19:180–188. doi:10.1016/j.tcb.2009.02.002
56. Murata T, Hasebe M (2007) Microtubule-dependent microtubule nucleation in plant cells. J Plant Res 120:73–78. doi:10.1007/s10265-006-0054-z
57. Murata T, Sonobe S, Baskin TI et al (2005) Microtubule-dependent microtubule nucleation based on recruitment of gamma-tubulin in higher plants. Nat Cell Biol 7:961–968. doi:10.1038/ncb1306
58. Murata T, Tanahashi T, Nishiyama T et al (2007) How do plants organize microtubules without a centrosome? J Integr Plant Biol 49:1154–1163. doi:10.1111/j.1672-9072.2007.00545.x
59. Murata T, Sano T, Sasabe M (2013) Mechanism of microtubule array expansion in the cytokinetic phragmoplast. Nature 4:1967. doi:10.1038/ncomms2967
60. Nakaoka Y, Miki T, Fujioka R et al (2012) An inducible RNA interference system in Physcomitrella patens reveals a dominant role of augmin in phragmoplast microtubule generation. Plant Cell 24:1478–1493. doi:10.1105/tpc.112.098509
61. Nislow C, Lombillo V, Kuriyama R, Mclntosh J (1992) A plus-end-directed motor enzyme that moves antiparallel microtubules in vitro localizes to the interzone of mitotic spindles. Nature 359:543–547
62. Nunes Bastos R, Gandhi SR, Baron RD et al (2013) Aurora B suppresses microtubule dynamics and limits central spindle size by locally activating KIF4A. J Cell Biol 202:605–621. doi:10.1083/jcb.201301094
63. Ota T (1961) The role of cytoplasm in cytokinesis of plant cells. Cytologia (Tokyo) 26:428–447
64. Otegui M, Staehelin L (2000) Cytokinesis in flowering plants: more than one way to divide a cell. Curr Opin Plant Biol 3:493–502
65. Otegui MS, Verbrugghe KJ, Skop AR (2005) Midbodies and phragmoplasts: analogous structures involved in cytokinesis. Trends Cell Biol 15:404–413. doi:10.1016/j.tcb.2005.06.003
66. Peterman EJG, Scholey JM (2009) Mitotic microtubule crosslinkers: insights from mechanistic studies. Curr Biol 19:R1089–R1094. doi:10.1016/j.cub.2009.10.047
67. Petry S, Groen AC, Ishihara K et al (2013) Branching microtubule nucleation in Xenopus egg extracts mediated by augmin and TPX2. Cell 152:768–777. doi:10.1016/j.cell.2012.12.044
68. Pickett-heaps AJD, Gunning BES, Brown RC et al (1999) The cytoplast concept in dividing plant cells: cytoplasmic domains and the evolution of spatially organized cell division. Am J Bot 86:153–172
69. Portran D, Zoccoler M, Gaillard J et al (2013) MAP65/Ase1 promote microtubule flexibility. Mol Biol Cell 24:1964–1973
70. Rasmussen CG, Wright AJ, Müller S (2013) The role of the cytoskeleton and associated proteins in determination of the plant cell division plane. Plant J 75:258–269. doi:10.1111/tpj.12177
71. Roll-Mecak A, McNally FJ (2010) Microtubule-severing enzymes. Curr Opin Cell Biol 22:96–103
72. Sano T, Higaki T, Oda Y et al (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. doi:10.1111/j.1365-313X.2005.02558.x
73. Sasabe M, Machida Y (2012) Regulation of organization and function of microtubules by the mitogen-activated protein kinase cascade during plant cytokinesis. Cytoskeleton (Hoboken) 69:913–918. doi:10.1002/cm.21072
74. Sasabe M, Machida Y, Yuji T et al (2006a) MAP65: a bridge linking a MAP kinase to microtubule turnover. Curr Opin Plant Biol 9:563–570. doi:10.1016/j.pbi.2006.09.010
75. Sasabe M, Soyano T, Takahashi Y et al (2006b) 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 20:1004–1014. doi:10.1101/gad.1408106.cells
76. Smertenko AP, Piette B, Hussey PJ (2011) The origin of phragmoplast asymmetry. Curr Biol 21:1924–1930. doi:10.1016/j.cub.2011.10.012
77. Smith LG (2001) Plant cell division: building walls in the right places. Nat Rev Mol Cell Biol 2:33–39. doi:10.1038/35048050
78. Subramanian R, Kapoor TM (2012) Building complexity: insights into self-organized assembly of microtubule-based architectures. Dev Cell 23:874–885. doi:10.1016/j.devcel.2012.10.011
79. Subramanian R, Ti S-C, Tan L et al (2013) Marking and measuring single microtubules by PRC1 and kinesin-4. Cell 154:377–390. doi:10.1016/j.cell.2013.06.021
80. Teixidó-Travesa N, Roig J, Lüders J (2012) The where, when and how of microtubule nucleation—one ring to rule them all. J Cell Sci 125:4445–4456. doi:10.1242/jcs.106971
81. Tindemans SH, Hawkins RJ, Mulder BM (2010) Survival of the aligned: ordering of the plant cortical microtubule array. Phys Rev Lett. doi:10.1103/PhysRevLett.104.058103
82. Uehara R, Goshima G (2010) Functional central spindle assembly requires de novo microtubule generation in the interchromosomal region during anaphase. J Cell Biol 191:259–267. doi:10.1083/jcb.201004150
83. Van Damme D (2009) Division plane determination during plant somatic cytokinesis. Curr Opin Plant Biol 12:745–751. doi:10.1016/j.pbi.2009.09.014
84. Van Damme D, Vanstraelen M, Geelen D (2007) Cortical division zone establishment in plant cells. Trends Plant Sci 12:458–464. doi:10.1016/j.tplants.2007.08.011
85. Van Lammeren AA, Keijzer CJ, Willemse MT, Kieft H (1985) Structure and function of the microtubular cytoskeleton during pollen development in Gasteria verrucosa (Mill.) H. Duval. Planta 165:1–11. doi:10.1007/BF00392205
86. Vanstraelen M, Van Damme D, De Rycke R et al (2006) Cell cycle-dependent targeting of a kinesin at the plasma membrane demarcates the division site in plant cells. Curr Biol 16:308–314. doi:10.1016/j.cub.2005.12.035
87. Vos JW, Dogterom M, Emons AMC (2004) Microtubules become more dynamic but not shorter during preprophase band formation: a possible “search-and-capture” mechanism for microtubule translocation. Cell Motil Cytoskelet 57:246–258
88. Vos JW, Pieuchot L, Evrard J-L et al (2008) The plant TPX2 protein regulates prospindle assembly before nuclear envelope breakdown. Plant Cell 20:2783–2797. doi:10.1105/tpc.107.056796
89. Wainman A, Buster DW, Duncan T et al (2009) A new Augmin subunit, Msd1, demonstrates the importance of mitotic spindle-templated microtubule nucleation in the absence of functioning centrosomes. Genes Dev 23:1876–1881. doi:10.1101/gad.532209
90. Walker KL, Müller S, Moss D et al (2007) Arabidopsis TANGLED identifies the division plane throughout mitosis and cytokinesis. Curr Biol 17:1827–1836. doi:10.1016/j.cub.2007.09.063
91. Wasteneys GO (2002) Microtubule organization in the green kingdom: chaos or self-order? J Cell Sci 115:1345–1354
92. Wightman R, Turner SR (2007) Severing at sites of microtubule crossover contributes to microtubule alignment in cortical arrays. Plant J 52:742–751
93. Wightman R, Chomicki G, Kumar M et al (2013) SPIRAL2 determines plant microtubule organization by modulating microtubule severing. Curr Biol 23:1902–1907
94. Xu XM, Zhao Q, Rodrigo-Peiris T et al (2008) RanGAP1 is a continuous marker of the Arabidopsis cell division plane. Proc Natl Acad Sci U S A 105:18637–18642. doi:10.1073/pnas.0806157105
95. Yasuhara H, Shibaoka H (2000) Inhibition of cell-plate formation by brefeldin A inhibited the depolymerization of microtubules in the central region of the phragmoplast. Plant Cell Physiol 41:300–310
96. Yasuhara H, Sonobe S, Shibaoka H (1993) Effects of taxol on the development of the cell plate and of the phragmoplast in tobacco BY-2 cells. Plant Cell Physiol 34:21–29
97. Zeng CJT, Lee Y-RJ, Liu B (2009) The WD40 repeat protein NEDD1 functions in microtubule organization during cell division in Arabidopsis thaliana. Plant Cell 21:1129–1140. doi:10.1105/tpc.109.065953
98. Zhang Q, Fishel E, Bertroche T, Dixit R (2013) Microtubule severing at crossover sites by katanin generates ordered cortical microtubule arrays in arabidopsis. Curr Biol 23:2191–2195