Summary.
In most higher-plant cells, cortical microtubules form a tightly focused preprophase band (PPB) that disappears with the onset of prometaphase, but whose location defines the future location of the cell plate at the end of cytokinesis. It is unclear whether the PPB microtubules themselves designate the precise area where the cell plate will insert, or rather if these microtubules are responding to a hierarchical signal(s). Here we show that narrowing of the microtubules within the PPB zone is not necessary for proper division plane determination. In cultured tobacco BY-2 cells in which PPB microtubules are depolymerized, the phragmoplast can still accurately locate and insert at the proper site. The data do not support a role for PPB microtubule narrowing in focusing the signal that is used later by the phragmoplast to position the cell plate; rather, proper phragmoplast positioning is more likely a consequence of a non-microtubule positional element. Although the PPB microtubules do not directly mark the division site, we show that they are required for accurate spindle positioning, an activity that presets the future growth trajectory of the phragmoplast and is necessary for insuring high-fidelity cell plate positioning.
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Abbreviations
- GFP-MBD:
-
green fluorescent protein fused to the microtubule binding domain of MAP4
- PPB:
-
preprophase band
References
P Apostolakos B Galatis (1987) ArticleTitleInduction, polarity and spatial control of cytokinesis in some abnormal subsidiary cell mother cells of Zea mays. Protoplasma 140 26–42 Occurrence Handle10.1007/BF01273253
J Bowser ASN Reddy (1997) ArticleTitleLocalization of a kinesin-like calmodulin-binding protein in dividing cells of Arabidopsis and tobacco. Plant J 12 1429–1437 Occurrence Handle10.1046/j.1365-313x.1997.12061429.x Occurrence Handle9450347 Occurrence Handle1:CAS:528:DyaK1cXlvVWhsg%3D%3D
C Camilleri J Azimzadeh M Pastuglia C Bellini O Grandjean D Bouchez (2002) ArticleTitleThe Arabidopsis TONNEAU2 gene encodes a putative novel protein phosphatase 2A regulatory subunit essential for the control of the cortical cytoskeleton. Plant Cell 14 833–845 Occurrence Handle10.1105/tpc.010402 Occurrence Handle11971138 Occurrence Handle1:CAS:528:DC%2BD38XjsFWksbc%3D
A Cleary L Smith (1998) ArticleTitleThe Tangled 1 gene is required for spatial control of cytoskeletal arrays associated with cell division during maize leaf development. Plant Cell 10 1875–1888 Occurrence Handle10.1105/tpc.10.11.1875 Occurrence Handle9811795 Occurrence Handle1:CAS:528:DyaK1MXptVOm
– 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
SR Cutler DW Ehrhardt (2002) ArticleTitlePolarized cytokinesis in vacuolate cells of Arabidopsis. Proc Natl Acad Sci USA 99 2812–2817 Occurrence Handle10.1073/pnas.052712299 Occurrence Handle11880633 Occurrence Handle1:CAS:528:DC%2BD38Xit1CrtL4%3D
P Dhonukshe TW Gadella SuffixJr (2003) ArticleTitleAlteration of microtubule dynamic instability during preprophase band formation revealed by yellow fluorescent protein-CLIP170 microtubule plus-end labeling. Plant Cell 15 597–611 Occurrence Handle12615935 Occurrence Handle1:CAS:528:DC%2BD3sXisVektL8%3D
R Dixit RJ Cyr (2002) ArticleTitleSpatio-temporal relationship between nuclear-envelope breakdown and preprophase band disappearance in cultured tobacco cells. Protoplasma 219 116–121 Occurrence Handle10.1007/s007090200012 Occurrence Handle11926062 Occurrence Handle1:STN:280:DC%2BD387ptlOiuw%3D%3D
B Galatis P Apostolakos C Katsaros (1983) ArticleTitleSynchronous organization of two preprophase microtubule bands and final cell plate arrangement in subsidiary cell mother cells of some Triticum species. Protoplasma 117 24–39 Occurrence Handle10.1007/BF01281781
CL Granger RJ Cyr (2000) ArticleTitleMicrotubule reorganization in tobacco BY-2 cells stably expressing GFP-MBD. Planta 210 502–509 Occurrence Handle10.1007/s004250050037 Occurrence Handle10750909 Occurrence Handle1:CAS:528:DC%2BD3cXhtVKitr0%3D
– – (2001) Use of abnormal preprophase bands to decipher division plane determination. J Cell Sci 114: 599–607
T Kakimoto H Shibaoka (1987) ArticleTitleActin filaments and microtubules in the preprophase band and phragmoplast of tobacco cells. Protoplasma 140 151–156 Occurrence Handle10.1007/BF01273724
B Liu J Marc HC Joshi BA Palevitz (1993) ArticleTitleA γ-tubulin-related protein associated with the microtubule arrays of higher plants in a cell cycle-dependent manner. J Cell Sci 104 1217–1228 Occurrence Handle7686171 Occurrence Handle1:CAS:528:DyaK3sXltlGkt70%3D
J Mathur (2004) ArticleTitlePlant cytoskeleton: reinforcing lines of division in plant cells. Curr Biol 14 R287–R289 Occurrence Handle10.1016/j.cub.2004.03.027 Occurrence Handle15062125 Occurrence Handle1:CAS:528:DC%2BD2cXivVKlu7o%3D
Y Mineyuki (1999) ArticleTitleThe preprophase band of microtubules: its function as a cytokinetic apparatus in higher plants. Int Rev Cytol 187 1–49 Occurrence Handle10.1016/S0074-7696(08)62415-8
– Palevitz BA (1990) Relationship between preprophase band organization, F-actin and the division site in Allium: fluorescence and morphometric studies on cytochalasin treated cells. J Cell Sci 97: 283–295
– Marc J, Palevitz BA (1989) Development of the preprophase band from random cytoplasmic microtubules in guard mother cells of Allium cepa L. Planta 178: 291–296
– Murata T, Wada M (1991a) Experimental obliteration of the preprophase band alters the site of cell division, cell plate orientation and phragmoplast expansion in Adiantum protonemata. J Cell Sci 100: 551–557
– Yamashita M, Nagahama Y (1991b) p34 cdc2 kinase homologue in the preprophase band. Protoplasma 162: 182–186
S Muller A Smertenko V Wagner M Heinrich PJ Hussey MT Hauser (2004) ArticleTitleThe plant microtubule-associated protein AtMAP65-3/PLE is essential for cytokinetic phragmoplast function. Curr Biol 14 412–417 Occurrence Handle10.1016/j.cub.2004.02.032 Occurrence Handle15028217 Occurrence Handle1:CAS:528:DC%2BD2cXisVektr8%3D
T Murata M Wada (1991) ArticleTitleEffects of centrifugation on preprophase-band formation in Adiantum protonemata. Planta 183 391–398 Occurrence Handle10.1007/BF00197738
BA Palevitz (1987) ArticleTitleActin in the preprophase band of Allium cepa. J Cell Biol 104 1515–1519 Occurrence Handle10.1083/jcb.104.6.1515 Occurrence Handle3294855 Occurrence Handle1:CAS:528:DyaL2sXksFGktL8%3D
S Patel R Annkatrin T Meulia R Dixit R Cyr I Meier (2004) ArticleTitleArabidopsis WPP-domain proteins are developmentally associated with the nuclear envelope and promote cell division. Plant Cell 16 3260–3273 Occurrence Handle10.1105/tpc.104.026740 Occurrence Handle15548735 Occurrence Handle1:CAS:528:DC%2BD2MXhtVKmtA%3D%3D
J Pickett-Heaps (1969a) ArticleTitlePreprophase microtubules and stomatal differentiation; some effects of centrifugation on symmetrical and asymmetrical cell division. J Ultrastruct Res 27 24–44
– (1969b) Preprophase microtubules and stomatal differentiation in Commelina cyanea. Aust J Biol Sci 22: 375–391
– (1974) Plant microtubules. In: Robards AW (ed) Dynamic aspects of plant ultrastructure. McGraw-Hill, New York, pp 219–255
J Pickett-Heaps DH Northcote (1966) ArticleTitleOrganization of microtubules and endoplasmic reticulum during mitosis and cytokinesis in wheat meristems. J Cell Sci 1 109–120 Occurrence Handle5929804 Occurrence Handle1:STN:280:CCmC387gtlw%3D
JM Segui-Simarro JR Austin EA White LA Staehelin (2004) ArticleTitleElectron tomographic analysis of somatic cell plate formation in meristematic cells of arabidopsis preserved by high-pressure freezing. Plant Cell 16 836–856 Occurrence Handle10.1105/tpc.017749 Occurrence Handle15020749 Occurrence Handle1:CAS:528:DC%2BD2cXjt1ynsLw%3D
EA Smirnova AS Bajer (1994) ArticleTitleMicrotubule converging centers and reorganization of the interphase cytoskeleton and the mitotic spindle in higher plant Haemanthus. Cell Motil Cytoskeleton 27 219–233 Occurrence Handle10.1002/cm.970270304 Occurrence Handle8020108 Occurrence Handle1:STN:280:ByuB1M7itFY%3D
LG Smith SM Gerttula S Han J Levy (2001) ArticleTitleTangled1: a microtubule binding protein required for the spatial control of cytokinesis in maize. J Cell Biol 152 231–236 Occurrence Handle10.1083/jcb.152.1.231 Occurrence Handle11149933 Occurrence Handle1:CAS:528:DC%2BD3MXjslyhtw%3D%3D
– Hake S, Sylvester AW (1996) The tangled-1 mutation alters cell division orientations throughout maize leaf development without altering leaf shape. Development 122: 481–489
LA Staehelin PK Hepler (1996) ArticleTitleCytokinesis in higher plants. Cell 84 821–824 Occurrence Handle10.1016/S0092-8674(00)81060-0 Occurrence Handle8601305 Occurrence Handle1:CAS:528:DyaK28XhvFKjsrw%3D
JA Traas JH Doonan DJ Rawlins PJ Shaw J Watts CW Lloyd (1987) ArticleTitleAn actin network is present in the cytoplasm throughout the cell cycle of carrot cells and associates with the nucleus. J Cell Biol 105 387–395 Occurrence Handle10.1083/jcb.105.1.387 Occurrence Handle2440896 Occurrence Handle1:CAS:528:DyaL2sXltlWiu70%3D
– Bellini C, Nacry P, Kronenberger J, Bouchez D, Caboche M (1995) Normal differentiation patterns in plants lacking microtubular preprophase bands. Nature 375: 676–677
D Twell SK Park TJ Hawkins D Schubert R Schmidt A Smertenko PJ Hussey (2002) ArticleTitleMOR1/GEM1 has an essential role in the plant-specific cytokinetic phragmoplast. Nat Cell Biol 4 711–714 Occurrence Handle10.1038/ncb844 Occurrence Handle12198497 Occurrence Handle1:CAS:528:DC%2BD38Xms1ahtb8%3D
JW Vos M Dogterom AM Emons (2004) ArticleTitleMicrotubules become more dynamic but not shorter during preprophase band formation: a possible “search-and-capture” mechanism for microtubule translocation. Cell Motil Cytoskeleton 57 246–258 Occurrence Handle10.1002/cm.10169 Occurrence Handle14752808
M Weingartner P Binarova D Drykova A Schweighofer JP David E Heberle-Bors J Doonan L Bogre (2001) ArticleTitleDynamic recruitment of Cdc2 to specific microtubule structures during mitosis. Plant Cell 13 1929–1943 Occurrence Handle10.1105/tpc.13.8.1929 Occurrence Handle11487703 Occurrence Handle1:CAS:528:DC%2BD3MXmsFKhsr4%3D
S Wick J Duniec (1984) ArticleTitleImmunofluorescence microscopy of tubulin and microtubule arrays in plant cells. II. Transition between the pre-prophase band and the mitotic spindle. Protoplasma 122 45–55 Occurrence Handle10.1007/BF01279436
H Yasuhara S Sonobe H Shibaoka (1993) ArticleTitleEffects of taxol on the development of the cell plate and of the phragmoplast in tobacco BY-2 cells. Plant Cell Physiol 34 21–29 Occurrence Handle1:CAS:528:DyaK3sXht1Wju7k%3D
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Correspondence and reprints: Department of Biology, Pennsylvania State University, University Park, PA 16802, U.S.A.
Present address: Winship Cancer Institute, Emory University School of Medicine, Atlanta, Georgia, U.S.A.
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Marcus, A., Dixit, R. & Cyr, R. Narrowing of the preprophase microtubule band is not required for cell division plane determination in cultured plant cells. Protoplasma 226, 169–174 (2005). https://doi.org/10.1007/s00709-005-0119-1
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DOI: https://doi.org/10.1007/s00709-005-0119-1