Microtubule plus-ends reveal essential links between intracellular polarization and localized modulation of endocytosis during division-plane establishment in plant cells
© Dhonukshe et al; licensee BioMed Central Ltd. 2005
Received: 26 January 2005
Accepted: 14 April 2005
Published: 14 April 2005
A key event in plant morphogenesis is the establishment of a division plane. A plant-specific microtubular preprophase band (PPB) accurately predicts the line of cell division, whereas the phragmoplast, another plant-specific array, executes cell division by maintaining this predicted line. Although establishment of these specific arrays apparently involves intracellular repolarization events that focus cellular resources to a division site, it still remains unclear how microtubules position the cell division planes. Here we study GFP-AtEB1 decorated microtubule plus-ends to dissect events at the division plane.
Early mitotic events included guided growth of endoplasmic microtubules (EMTs) towards the PPB site and their coincident localization with endocytic vesicles. Consequently, an endosomal belt lay in close proximity to the microtubular PPB at its maturation and was maintained during spindle formation. During cytokinesis, EMTs radiated from the former spindle poles in a geometrical conformation correlating with cell-plate navigation and tilt-correction. Naphthylphtalamic acid (NPA), an inhibitor of polar auxin efflux, caused abnormal PPBs and shifted division planes.
Our observations reveal a spatio-temporal link between microtubules and intracellular polarization essential for localized endocytosis and precise establishment of the division plane in plants. Additionally, they implicate the growth regulator, auxin, in this important cellular event.
In cell wall-encased, immobile plant cells, tight regulation of the cell division plane plays a crucial role in tissue and organ morphogenesis [1, 2]. At the onset of mitosis a plant-specific cortical microtubule array, the PPB , emerges. Although the PPB disassembles as the cell enters mitosis, it precisely predicts where the new cell plate attaches to the parental cell walls at the end of cytokinesis [1, 2]. Cell division planes are drastically affected by the absence of PPB , which may be achieved through experimental obliteration  or through genetic defects . Since the discovery of the PPB four decades ago, the mechanism governing its creation and effect on delineating the future cell division plane has remained a mystery.
Though initially considered to be a cortical process, PPB formation involves two coincident cytoplasmic events too, namely the migration of the nucleus towards the cell center , and recruitment of numerous EMTs within motile cytoplasmic strands [8, 9]. In centrifuged protonemata (consisting of a single elongated cell), nuclear displacement prior to pre-prophase induces the formation of a PPB around the new nuclear position, suggesting a role for the nucleus in PPB placement . However, in plant cells under normal gravity conditions, the nucleus is positioned by microtubules, since its random migration is prevented by microtubular depolymerization . These observations point towards a functional connection between the nucleus, microtubules and cell cortex for marking the PPB. In budding yeast, EMTs play a role in bringing the nucleus to the division plane by a cortical 'search and capture' mechanism [12–14]; and in fission yeast, EMTs position the nucleus by pushing against the cortex . Under in vitro, simulated conditions, the microtubule seeds also probe the metallic boundaries of artificial chambers with cellular dimensions to bring nuclei to the center . Together, these studies on diverse systems corroborate the role of microtubules in probing the cellular geometry to settle the nucleus at the center of the cell. In the absence of information on the polarity and dynamics of plant EMTs, their precise role in association with the nucleus and the PPB is unclear.
In plants, in addition to the PPB, the other two mitotic microtubular arrays, the spindle and the phragmoplast microtubules, are also of endoplasmic nature. During the spindle stage, the perpendicularity of the spindle to the cell division plane is often lost because of its rotation. In mammalian and yeast cells the spindle is kept at the center of the cell or at the bud site by the centrosome-originating astral microtubules [17, 18]. In addition, any error in spindle orientation in these cell types is corrected by the outgoing astral microtubules, which probe the cortex to ensure that the segregated chromosomes are sufficiently distant and are not cleaved by the constricting actomyosin ring [19, 20]. In acentrosomal plant cells, after PPB breakdown and disappearance of the nuclear surface-bound EMT, the factors maintaining the spindle at the cell centre still remain unresolved. Paradoxically, in plant cells possessing disoriented spindles, the cell plates are still able to anchor properly to the division sites marked perpendicularly to the cell axis. A mechanism obviously exists in plant cells to correct spindle disorientation and reinforce the line of cell division, but it remains obscure.
Here, we investigated the role of EMTs during PPB formation and their subsequent behavior following karyokinesis. Because of their uniform cell size, continuous cell division activity and absence of background fluorescence, Tobacco BY-2 cell suspensions remain a system of choice for plant cell cycle studies . Therefore, we used tobacco BY-2 cells stably transformed with different microtubular markers, and performed a live cell time-lapse analysis to elucidate the role of EMTs in reinforcing the lines of the cell division planes in plants.
GFP-AtEB1 labeled plant microtubule plus ends exhibit guided growth to create bundles
General observations on microtubule guidance and bundling formed the basis of our subsequent experiments. Tracking the GFP-AtEB1 comets, it was found that >80 % of freshly polymerizing microtubules exhibited guided growth on tracks established by existing microtubules, thereby creating bundles of microtubules (Figure 1C; see also additional file 2: Movie 2). Preexisting microtubule-guided oriented bundling often involved i) two or more microtubules with apparently similar polarity moving one after the other, ii) microtubules with presumably opposite polarities moving in opposite directions to each other or iii) independent microtubules moving together as a pair with similar velocities (4.15 ± 0.41 μm/min, n = 29) (Figure 1B; see also additional file 1: Movie 1). Although mammalian EB1 often induces microtubule bundling upon overexpression, AtEB1 did not cause the observed bundling in the plant cells since it lacks the microtubule bundling domain present in the mammalian ortholog . Instead, intermicrotubular bridges  might be responsible for the observed bundle formation. In addition, when two microtubules grew together side-by-side on the same track, it was frequently observed that one of them shrank while the other continued growing (see additional file 1: Movie 1). Further information on microtubular guidance and bundling mechanisms came from analysis of cells coexpressing GFP-AtEB1 and YFP-MAP4. A growing microtubule (green arrow, Figure 1E) could detach from an existing track and move on to another track where its growth became guided in another direction (Figure 1E). Interphase microtubules in mammalian cells show a similar guidance mechanism . We also observed individual microtubule plus ends approaching each other from a similar (Figure 1F) or opposite (Figure 1G) direction and meeting without inducing catastrophe. Strikingly, microtubular nucleation was sometimes initiated on an existing microtubule (Figure 1H), an observation consistent with the plant-specific localization of gamma tubulin along the microtubule length  and with a study reporting microtubule nucleation from stable tubulin oligomers . Microtubules also changed trajectories by reorienting their minus or plus ends when one of the ends was supported on the other polymer (Figure 1I, J). It was also observed that motile polymers exhibiting specialized treadmilling  initiated bundling by bridging the two preexisting and separate polymers (Figure 1K). In cases of guided growth-induced bundling, a shorter microtubule could adopt the growth direction of a preexisting longer microtubule and vice versa (Figure 1L). When one of the microtubules in a bundle retracted, it frequently caused the other to bend, implying the exertion of a pulling force (Figure 1M). We also observed that upon release of a minus end from a nucleation site, the opposite plus end depolymerized (with concomitant loss of GFP-AtEB1), whereas upon acquisition of a new support by its minus end the microtubule retained growth (and regained GFP-AtEB1) (Figure 1N). These observations indicate a provision for new nucleation on existing polymers, while suggesting that in certain cases the plus end somehow 'senses' the physical state of the opposite minus end. Together, these findings implicate intermicrotubular affinities and the capacity of the polymers to nucleate new or detached microtubules as a general mode of microtubule survival, reorientation and bundle creation.
Emergence, polarity and dynamics of EMTs at the onset of cell division
Role of EMTs in premitotic cytoplasmic organization
Guided growth of EMTs towards the PPB site and their coincident localization with endocytic vesicles
EMTs radiating from the former spindle poles attain a geometrical conformation correlating with cell-plate navigation and tilt-correction
Following observations on microtubule and organelle behavior during the early stages of mitosis, we analyzed events at later stages. Immediately after chromosomal separation at anaphase, the EMTs emanating from the region occupied by spindle poles 'probed' the cell cortex (Figure 5B, C; see also additional file 9: Movie 9) while exhibiting unidirectional growth at speeds of 8.52 ± 1.23 μm/min (n = 45). During late telophase, these EMTs mainly probed the cortical areas previously occupied by the PPB (Figure 5D). In addition, the EMTs originating from the non-facing surfaces of the daughter nuclei appeared fewer than the phragmoplast microtubules and occasionally exhibited growth trajectories towards the cell poles (Figure 5E). Because of the remarkable co-incidence between the EMTs and endocytosed material during preprophase, we investigated whether these EMTs approaching the cortex co-localized with FM4-64-labeled endocytic material during telophase. Such co-localization was observed both for GFP-MAP4 (Figure 5F–I) and GFP-AtEB1 (Figure 5J–M) labeled EMTs which were approaching the former PPB sites. During cell plate expansion, the EMTs appeared to navigate the cell plate and to align it to establish a clear line of division (Figure 5N, O; see also additional file 10: Movie 10). EMT plus ends within the phragmoplast midline (where the cell plate subsequently formed) were labeled strongly with GFP-AtEB1 but less strongly with YFP-MAP4, indicating the polarity of the phragmoplast microtubules, oriented with their plus ends towards the developing cell plate (Figure 5P).
In budding yeast, cytokinesis is delayed until the spindle is properly positioned, but in a mutant for Bim1 (EB1 homologue) this delay is abolished, resulting in abnormal cell division . This suggests that Bim1 has an important role in sensing and positioning the spindle. Cytokinesis in plants often begins with tilted spindles, indicating the absence of a spindle alignment checkpoint in plant cells. However, this spindle tilting is corrected later during the progression of cytokinesis, which may indicate the involvement of a positioning sensor and correction mechanism in plant cells. We propose that the EMTs initiating from the spindle poles and approaching the cortex (Figure 5B–O) are involved in this sensor and tilting mechanism. Though different scenarios can be evoked for the correction mechanism, in each case a specialized cortical reference site would be required. We therefore investigated the effect of an auxin efflux inhibitor, NPA, which has been shown to block both vesicular trafficking and internalization of plasma membrane-localized proteins  without directly affecting microtubules or actin filaments .
Polarity inhibitor induces abnormal PPBs and shifts cell division planes
In mammalian and yeast cells, a microtubule plus end-mediated 'search and capture' mechanism has been credited with positioning and aligning the spindles [17, 19] and determining the plane of cell division . Our observations suggest that EMTs in plant cells may behave similarly to establish and regulate the cell division plane. Interestingly, it has been shown previously that injuries caused by inserting microneedles at these specific cortical sites, probed by EMTs during cytokinesis, affect cell plate alignment .
In mammalian and yeast cells, EB1 binds to adenomatous polyposis coli (APC). In epithelial cells, APC is mainly found at specialized cortical sites , providing a planar cue . In mammalian cells, microtubule-mediated APC delivery to specialized cortical sites has been demonstrated [44, 45]. A mechanism for attaining polarity cues is proposed for mammalian cells, according to which the EB1-labeled microtubule plus ends target to the specialized APC-marked cortical sites . A similar role in attracting EB1-labeled microtubular plus ends towards the cortex has been attributed to Kar9p in budding yeast  and to Moe1 in fission yeast . Moreover, it has been suggested that LIS1 is a regulated adapter between CLIP170 and cytoplasmic dynein at sites involved in cargo-microtubule loading and/or the control of microtubule dynamics .
Interestingly, plants seem to possess homologues for APC, Kar9p and Moe1, and the plant cytoskeletal-related Tonneau2  protein contains a LisH domain present in LIS1 (our unpublished results based on the NCBI search engine). In maize, the Tangled1 (which is distantly related to the APC) mutant displays altered PPBs, spindles and phragmoplasts and shifted cell division planes. Furthermore, Tangled1 expression and its microtubule localization correlate with the cell division stage . In mammalian cells, EB1 is required for microtubule tip-specific localization of APC but not vice versa. In the absence of EB1, APC localizes all along the microtubule lengths [50, 51]. In addition, APC assembly in the cortical clusters is EB1-independent but depends on the existence of the armadillo domain . In plants, it remains to be determined how EB1 localizes in the Tangled1 mutant and vice versa. From parallels in the mammalian cell literature one might hypothesize that Tangled1-mediated EB1 targeting to specialized cortical sites regulates the cell division planes in plants. However, there are several problems with this hypothesis. For instance, Tangled1 contains only the microtubule binding domain and lacks both the EB1 binding and the armadillo domains of APC . Inversely, AtEB1 possesses an APC interaction domain  and a unique C-terminal acidic tail , and armadillo domain-containing proteins exist in Arabidopsis . This leaves open the possibility that EB1 interacts with other PM-localized basic protein(s). In addition, plants lacking Tonneau2 fail to assemble PPB  and Tonneau2 possesses a LisH domain. From the parallel mammalian cell literature one might hypothesize that the LisH domain in Tonneau2 may mediate EMT plus end cortical interactions. Hence it will be interesting to determine how EB1 localizes in Tangled1 and Tonneau2 mutants and vice versa.
In mammalian cells, many proteins have been shown to associate in a microtubule plus end complex, which has been described as a plus end raft . As with lipid rafts, protein concentration at the distal ends may allow a cascade of interactions in the restricted area of a microtubule plus end. This may, in turn, control the dynamic behavior of this cytoskeletal network and its anchoring to other structures . An alternative to this would be that EMTs, by interpreting cell geometry and polarity cues, deposit protein(s) at the PPB, which subsequently attracts the phragmoplast microtubules. Conversely, the connection between EMT plus ends and endocytosis may indicate a role for localized endocytosis in modifying the PM architecture, which may transmit the memory for re-attracting EMT plus ends during cytokinesis. We consider that the polarity inhibitor NPA affects PPB formation by modulating endocytosis, as it does not affect microtubules but interferes with endocytosis and with polarity-based EMT plus end targeting to specialized areas of the PM. Thus, feedback loops, comprising polarity establishment-endocytosis-microtubule plus end guidance-further endocytosis, appear to be essential for defining and creating planes of cell division in plant cells.
In conclusion, our results suggest that in mitotic plant cells, EMT plus ends may act as cell shape/polarity sensing and orienting machines by their sustained cortical targeting, as shown for yeast [15, 55]. EMTs in premitotic plant cells are bundled and bidirectional, as reported very recently in fission yeast by analysis of the EB1 homologue mal3p , indicating evolutionary conservation of the processes involved in defining cell division planes. Importantly, we show that at preprophase the targeting of EMT plus ends coincides with endocytosis events to establish a plant-specific cortical endocytic belt. During cytokinesis, this same belt again interacts with the EMT plus ends of the expanding phragmoplast to ensure proper cell plate navigation and docking. Our results reveal a link between the position of EMT plus ends, the establishment of intracellular polarity and the localization of endocytosis that is essential for the regulation of cell division planes in plants.
Plant material and growth conditions
Tobacco BY-2 cells were cultured and transformed as reported previously .
Construction of reporter genes
The construction of GFP-MAP4, YFP-MAP4, YFP-CLIP170 and GFP-AtEB1 was described previously [9, 22]. GFP-Ara7 in vector pBSIIKS+  was excised with HindIII-XbaI and sub-cloned into the binary vector pBINPLUS. STtmd-YFP in vector pMON  was digested with PstI -SmaI and cloned into the binary vector pCAMBIA 1390.
Fluorescent dyes and drugs
FM4-64 (Molecular Probes) dissolved in water was applied to the BY-2 cells at 2 μM final concentration for 5 min. The cells were washed with BY-2 medium to remove excess dye and were observed immediately. Alexa 633 (Molecular probes) and Mitotracker (Molecular probes) dissolved in water were also applied at 2 μM final concentration and the cells were observed immediately. Stock solutions of taxol (Sigma-Aldrich), latrunculin B (Sigma-Aldrich) and NPA (Sigma-Aldrich) in DMSO were applied to the cells to give final concentrations of 10 μM, 10 μM and 50 μM respectively. Stock solutions of oryzalin (Greyhound Chromatography and Allied Chemicals, Merseyside, UK) were prepared in ethanol and used at 10 μM final concentration.
Live cell analysis
For live cell analysis, the Zeiss CLSM510 system implemented on an inverted (Axiovert 100) microscope was used. The microscopy system, sample preparation, single wavelength scanning, image processing and movie generation were as previously described . Dual color imaging was performed using dual excitation/emission scanning in multitracking mode. For GFP /YFP dual scanning, we used excitation/emission combinations of 458 nm/ BP 475–525 for GFP and 514 nm/ BP 530–600 for YFP, in combination with the HFT 458/514 primary and NFT515 secondary dichroic splitters. For GFP/ FM4-64 dual scanning, we used excitation/emission combinations of 488 nm/ BP 505–550 for GFP and 543 nm/ LP585 for FM4-64, in combination with the HFT 488/543 primary and NFT545 secondary dichroic splitters. For GFP/ Alexa dual scanning, we used excitation/emission combinations of 488 nm/ BP 505–550 for GFP and 633 nm/ LP650 for Alexa, in combination with the HFT UV/488/543/633 primary and NFT545 secondary dichroic splitters. All filters were from Zeiss. For time-lapse analysis, images were obtained at 1–10 s time intervals. All experiments were repeated 3–5 times. Acquired images were processed using LSM510 Image Browser version 3.0 (Zeiss Corp.). Maximum projections were obtained from 0.5 μm spaced serial optical sections and were exported as TIFF files. For time-series scans, all the images were exported as time-series TIFF files. The exported images were processed with Adobe Photoshop version 5.0 (Adobe Systems Inc.). For individual plant microtubule growth measurements, all time scans were analyzed in the animation mode of LSM510 Image Browser 3.2 (Zeiss Corp.) by marking the single ends of individual microtubules in each image by a zoom function and tracking them for several minutes. The shortest displacement of the plus ends resolvable in this analysis was 0.1 μm. The time values were obtained from the respective frame times in the time-lapse. Thereafter, the data were manually transferred into Excel and processed. The microtubule growth histories (kymographs) were obtained by processing the raw data in LSM510 Image Browser 3.2 (Zeiss Corp.).
We acknowledge F. Baluska for stimulating discussions. We are grateful to A. Nakano (RIKEN, Saitama, Japan) for the GFP-Ara7 construct and J. Carette (Wageningen Univ., the Netherlands) for the ST-YFP construct. P.D. and T.W.J.G. were supported by NWO FOM-ALW 805.47.012 and by NWO van der Leeuw 835.25.004. J. M. was supported by a Volkswagon Stiftung grant to M.H.
- Smith L: Plant cell division: building walls in the right places. Nat Rev Mol Cell Biol. 2001, 2: 33-40. 10.1038/35048050.View ArticlePubMedGoogle Scholar
- Mathur J: Plant cytoskeleton: reinforcing lines of division in plant cells. Curr Biol. 2004, 14: R287-289. 10.1016/j.cub.2004.03.027.View ArticlePubMedGoogle Scholar
- Pickett-Heaps JD, Northcote DH: Organization of microtubules and endoplasmic reticulum during mitosis and cytokinesis in wheat meristems. J Cell Sci. 1966, 1: 109-120.PubMedGoogle Scholar
- Traas J, Bellini C, Nacry P, Kronenberger J, Bouchez D, Caboche M: Normal differentiation patterns in plants lacking microtubular preprophase bands. Nature. 1995, 375: 676-677. 10.1038/375676a0.View ArticleGoogle Scholar
- Mineyuki Y: The Preprophase Band of Microtubules: Its Function as a Cytokinetic Apparatus in Higher Plants. Int Rev Cytol. 1999, 187: 1-49.View ArticleGoogle Scholar
- Cleary AL, Smith LG: The Tangled1 gene is required for spatial control of cytoskeletal arrays associated with cell division during maize leaf development. Plant Cell. 1998, 10: 1875-1888. 10.1105/tpc.10.11.1875.PubMed CentralView ArticlePubMedGoogle Scholar
- Sinnott EW, Bloch R: Cytoplasmic behaviour during division of vacuolate plant cells. Proc Natl Acad Sci U S A. 1940, 26: 223-227.PubMed CentralView ArticlePubMedGoogle Scholar
- Flanders DJ, Rawlins DJ, Shaw PJ, Lloyd CW: 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. 1990, 110: 1111-1122. 10.1083/jcb.110.4.1111.View ArticlePubMedGoogle Scholar
- Dhonukshe P, Gadella TW: Alteration of microtubule dynamic instability during preprophase band formation revealed by yellow fluorescent protein-CLIP170 microtubule plus-end labeling. Plant Cell. 2003, 15: 597-611. 10.1105/tpc.008961.PubMed CentralView ArticlePubMedGoogle Scholar
- Murata T, Wada M: Effects of centrifugation on preprophase-band formation in Adiantum protonemata. Planta. 1991, 183: 391-398. 10.1007/BF00197738.View ArticlePubMedGoogle Scholar
- Katsuta J, Hashiguchi Y, Shibaoka H: The role of the cytoskeleton in positioning of the nucleus in premitotic tobacco BY-2 cells. J Cell Sci. 1990, 95: 413-422.Google Scholar
- Adames NR, Cooper JA: Microtubule interactions with the cell cortex causing nuclear movements in Saccharomyces cerevisiae. J Cell Biol. 2000, 149: 863-874. 10.1083/jcb.149.4.863.PubMed CentralView ArticlePubMedGoogle Scholar
- Gundersen GG: Evolutionary conservation of microtubule-capture mechanisms. Nat Rev Mol Cell Biol. 2002, 3: 296-304. 10.1038/nrm777.View ArticlePubMedGoogle Scholar
- Mimori-Kiyosue Y, Tsukita S: "Search-and-capture" of microtubules through plus-end-binding proteins (+TIPs). J Biochem (Tokyo). 2003, 134: 321-326.View ArticleGoogle Scholar
- Tran PT, Marsh L, Doye V, Inoue S, Chang F: A mechanism for nuclear positioning in fission yeast based on microtubule pushing. J Cell Biol. 2001, 153: 397-411. 10.1083/jcb.153.2.397.PubMed CentralView ArticlePubMedGoogle Scholar
- Faivre-Moskalenko C, Dogterom M: Dynamics of microtubule asters in microfabricated chambers: the role of catastrophes. Proc Natl Acad Sci U S A. 2002, 99: 16788-16793. 10.1073/pnas.252407099.PubMed CentralView ArticlePubMedGoogle Scholar
- Lee L, Tirnauer JS, Li J, Schuyler SC, Liu JY, Pellman D: Positioning of the mitotic spindle by a cortical-microtubule capture mechanism. Science. 2000, 287: 2260-2262. 10.1126/science.287.5461.2260.View ArticlePubMedGoogle Scholar
- Ahringer J: Control of cell polarity and mitotic spindle positioning in animal cells. Curr Opin Cell Biol. 2003, 15: 73-81. 10.1016/S0955-0674(02)00018-2.View ArticlePubMedGoogle Scholar
- Oliferenko S, Balasubramanian MK: Astral microtubules monitor metaphase spindle alignment in fission yeast. Nat Cell Biol. 2002, 4: 816-820. 10.1038/ncb861.View ArticlePubMedGoogle Scholar
- Wang H, Oliferenko S, Balasubramanian MK: Cytokinesis: relative alignment of the cell division apparatus and the mitotic spindle. Curr Opin Cell Biol. 2003, 15: 82-87. 10.1016/S0955-0674(02)00006-6.View ArticlePubMedGoogle Scholar
- Geelen DN, Inze DG: A bright future for the bright yellow-2 cell culture. Plant Physiol. 2001, 127: 1375-1379. 10.1104/pp.127.4.1375.PubMed CentralView ArticlePubMedGoogle Scholar
- Mathur J, Mathur N, Kernebeck B, Srinivas BP, Hulskamp M: A novel localization pattern for an EB1-like protein links microtubule dynamics to endomembrane organization. Curr Biol. 2003, 13: 1991-1997. 10.1016/j.cub.2003.10.033.View ArticlePubMedGoogle Scholar
- Bu W, Su LK: Characterization of functional domains of human EB1 family proteins. J Biol Chem. 2003, 278: 49721-49731. 10.1074/jbc.M306194200.View ArticlePubMedGoogle Scholar
- Chan J, Jensen CG, Jensen LC, Bush M, Lloyd CW: The 65-kDa carrot microtubule-associated protein forms regularly arranged filamentous cross-bridges between microtubules. Proc Natl Acad Sci U S A. 1999, 96: 14931-14936. 10.1073/pnas.96.26.14931.PubMed CentralView ArticlePubMedGoogle Scholar
- Krylyshkina O, Anderson KI, Kaverina I, Upmann I, Manstein DJ, Small JV, Toomre DK: Nanometer targeting of microtubules to focal adhesions. J Cell Biol. 2003, 161: 853-859. 10.1083/jcb.200301102.PubMed CentralView ArticlePubMedGoogle Scholar
- Drykova D, Cenklova V, Sulimenko V, Volc J, Draber P, Binarova P: Plant gamma-tubulin interacts with alphabeta-tubulin dimers and forms membrane-associated complexes. Plant Cell. 2003, 15: 465-480. 10.1105/tpc.007005.PubMed CentralView ArticlePubMedGoogle Scholar
- Caudron N, Arnal I, Buhler E, Job D, Valiron O: Microtubule nucleation from stable tubulin oligomers. J Biol Chem. 2002, 277: 50973-50979. 10.1074/jbc.M209753200.View ArticlePubMedGoogle Scholar
- Shaw SL, Kamyar R, Ehrhardt DW: Sustained microtubule treadmilling in Arabidopsis cortical arrays. Science. 2003, 300: 1715-1718. 10.1126/science.1083529.View ArticlePubMedGoogle Scholar
- Piehl M, Cassimeris L: Organization and dynamics of growing microtubule plus ends during early mitosis. Mol Biol Cell. 2003, 14: 916-925. 10.1091/mbc.E02-09-0607.PubMed CentralView ArticlePubMedGoogle Scholar
- Boevink P, Oparka K, Santa Cruz S, Martin B, Betteridge A, Hawes C: Stacks on tracks: the plant Golgi apparatus traffics on an actin/ER network. Plant J. 1998, 15: 441-447. 10.1046/j.1365-313X.1998.00208.x.View ArticlePubMedGoogle Scholar
- Schmit AC, Lambert AM: Characterization and dynamics of cytoplasmic F-actin in higher plant endosperm cells during interphase, mitosis, and cytokinesis. J Cell Biol. 1987, 105: 2157-2166. 10.1083/jcb.105.5.2157.View ArticlePubMedGoogle Scholar
- Mineyuki Y, Karahara I, Staehelin LA: Quantitative analysis of cytoskeletal arrays and endocytic vesicles in the cortex of dividing plant cells by dual-axis EM tomography. Procceedings of the 30th NIPS International Symposium, March 12–15, 2003. 2003, Okazaki, Japan, 120-121.Google Scholar
- Ueda T, Yamaguchi M, Uchimiya H, Nakano A: Ara6, a plant-unique novel type Rab GTPase, functions in the endocytic pathway of Arabidopsis thaliana. Embo J. 2001, 20: 4730-4741. 10.1093/emboj/20.17.4730.PubMed CentralView ArticlePubMedGoogle Scholar
- Nebenfuhr A, Frohlick JA, Staehelin LA: Redistribution of Golgi stacks and other organelles during mitosis and cytokinesis in plant cells. Plant Physiol. 2000, 124: 135-151. 10.1104/pp.124.1.135.PubMed CentralView ArticlePubMedGoogle Scholar
- Hoshino H, Yoneda A, Kumagai F, Hasezawa S: 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. 2003, 222: 157-165. 10.1007/s00709-003-0012-8.View ArticlePubMedGoogle Scholar
- Geldner N, Friml J, Stierhof YD, Jurgens G, Palme K: Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature. 2001, 413: 425-428. 10.1038/35096571.View ArticlePubMedGoogle Scholar
- Muhua L, Adames NR, Murphy MD, Shields CR, Cooper JA: A cytokinesis checkpoint requiring the yeast homologue of an APC-binding protein. Nature. 1998, 393: 487-491. 10.1038/31014.PubMed CentralView ArticlePubMedGoogle Scholar
- Petrasek J, Cerna A, Schwarzerova K, Elckner M, Morris DA, Zazimalova E: Do phytotropins inhibit auxin efflux by impairing vesicle traffic?. Plant Physiol. 2003, 131: 254-263. 10.1104/pp.012740.PubMed CentralView ArticlePubMedGoogle Scholar
- Petrasek J, Elckner M, Morris DA, Zazimalova E: Auxin efflux carrier activity and auxin accumulation regulate cell division and polarity in tobacco cells. Planta. 2002, 216: 302-308. 10.1007/s00425-002-0845-y.View ArticlePubMedGoogle Scholar
- Canman JC, Cameron LA, Maddox PS, Straight A, Tirnauer JS, Mitchison TJ, Fang G, Kapoor TM, Salmon ED: Determining the position of the cell division plane. Nature. 2003, 424: 1074-1078. 10.1038/nature01860.View ArticlePubMedGoogle Scholar
- Gunning BE, Wick SM: Preprophase bands, phragmoplasts, and spatial control of cytokinesis. J Cell Sci Suppl. 1985, 2: 157-179.View ArticlePubMedGoogle Scholar
- Nathke IS, Adams CL, Polakis P, Sellin JH, Nelson WJ: The adenomatous polyposis coli tumor suppressor protein localizes to plasma membrane sites involved in active cell migration. J Cell Biol. 1996, 134: 165-179. 10.1083/jcb.134.1.165.View ArticlePubMedGoogle Scholar
- Bienz M: Spindles cotton on to junctions, APC and EB1. Nat Cell Biol. 2001, 3: E67-68. 10.1038/35060140.View ArticlePubMedGoogle Scholar
- Askham JM, Moncur P, Markham AF, Morrison EE: Regulation and function of the interaction between the APC tumour suppressor protein and EB1. Oncogene. 2000, 19: 1950-1958. 10.1038/sj.onc.1203498.View ArticlePubMedGoogle Scholar
- Mimori-Kiyosue Y, Shiina N, Tsukita S: Adenomatous polyposis coli (APC) protein moves along microtubules and concentrates at their growing ends in epithelial cells. J Cell Biol. 2000, 148: 505-518. 10.1083/jcb.148.3.505.PubMed CentralView ArticlePubMedGoogle Scholar
- Lu B, Roegiers F, Jan LY, Jan YN: Adherens junctions inhibit asymmetric division in the Drosophila epithelium. Nature. 2001, 409: 522-525. 10.1038/35054077.View ArticlePubMedGoogle Scholar
- Chen CR, Chen J, Chang EC: A conserved interaction between Moe1 and Mal3 is important for proper spindle formation in Schizosaccharomyces pombe. Mol Biol Cell. 2000, 11: 4067-4077.PubMed CentralView ArticlePubMedGoogle Scholar
- Coquelle FM, Caspi M, Cordelieres FP, Dompierre JP, Dujardin DL, Koifman C, Martin P, Hoogenraad CC, Akhmanova A, Galjart N, et al: LIS1, CLIP-170's key to the dynein/dynactin pathway. Mol Cell Biol. 2002, 22: 3089-3102. 10.1128/MCB.22.9.3089-3102.2002.PubMed CentralView ArticlePubMedGoogle Scholar
- Camilleri C, Azimzadeh J, Pastuglia M, Bellini C, Grandjean O, Bouchez D: The Arabidopsis TONNEAU2 gene encodes a putative novel protein phosphatase 2A regulatory subunit essential for the control of the cortical cytoskeleton. Plant Cell. 2002, 14: 833-845. 10.1105/tpc.010402.PubMed CentralView ArticlePubMedGoogle Scholar
- Smith LG, Gerttula SM, Han S, Levy J: Tangled1: a microtubule binding protein required for the spatial control of cytokinesis in maize. J Cell Biol. 2001, 152: 231-236. 10.1083/jcb.152.1.231.PubMed CentralView ArticlePubMedGoogle Scholar
- Tirnauer JS, Bierer BE: EB1 proteins regulate microtubule dynamics, cell polarity, and chromosome stability. J Cell Biol. 2000, 149: 761-766. 10.1083/jcb.149.4.761.PubMed CentralView ArticlePubMedGoogle Scholar
- Barth AI, Siemers KA, Nelson WJ: Dissecting interactions between EB1, microtubules and APC in cortical clusters at the plasma membrane. J Cell Sci. 2002, 115: 1583-1590.PubMed CentralPubMedGoogle Scholar
- Coates JC: Armadillo repeat proteins: beyond the animal kingdom. Trends Cell Biol. 2003, 13: 463-471. 10.1016/S0962-8924(03)00167-3.View ArticlePubMedGoogle Scholar
- Galjart N, Perez F: A plus-end raft to control microtubule dynamics and function. Curr Opin Cell Biol. 2003, 15: 48-53. 10.1016/S0955-0674(02)00007-8.View ArticlePubMedGoogle Scholar
- Korinek WS, Copeland MJ, Chaudhuri A, Chant J: Molecular linkage underlying microtubule orientation toward cortical sites in yeast. Science. 2000, 287: 2257-2259. 10.1126/science.287.5461.2257.View ArticlePubMedGoogle Scholar
- Busch KE, Brunner D: The microtubule plus end-tracking proteins mal3p and tip1p cooperate for cell-end targeting of interphase microtubules. Curr Biol. 2004, 14: 548-559. 10.1016/j.cub.2004.03.029.View ArticlePubMedGoogle Scholar
- Carette JE, Stuiver M, Van Lent J, Wellink J, Van Kammen A: Cowpea mosaic virus infection induces a massive proliferation of endoplasmic reticulum but not Golgi membranes and is dependent on de novo membrane synthesis. J Virol. 2000, 74: 6556-6563. 10.1128/JVI.74.14.6556-6563.2000.PubMed CentralView ArticlePubMedGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.