Unique Characteristics of Cell Division in Vascular Plants

Abstract

In eukaryotes, both microtubules (MTs) and microfilaments (MFs) are cytoskeletal polymers involved in meristematic cell proliferation. While animal cells build their MT arrays from structured organelles, such as centrosomes, and while they depolymerise their MFs and become round during mitosis, vascular plant cells lack centrosomes, maintain a filamentous actin cage around the spindle and are surrounded by a cell wall, preventing cellular mobility. During the cell cycle, plants activate specific dispersed MT nucleating sites, revealing successive plant‐specific cytoskeletal arrays. The MF meshwork surrounding the spindle eventually drives the centrifugal growth of MTs, which leads Golgi‐derived vesicles to fuse and separate each daughter cell during cytokinesis. The main orientation of actin fibres is parallel to that of spindle MTs, while a perpendicular constriction ring ensures animal daughter cell separation. However, despite the differences in their cytoskeleton behaviour and dynamics, both cell types succeed in controlled chromosome segregation.

Key Concepts

  • Mitosis is a short cell cycle period during which the cytoskeleton ensures balanced segregation of duplicated sister chromatids into two daughter cells.
  • Plant cells have to deal with their pecto‐cellulosic cell wall, constraining the orientation of the division axis in order to control morphogenesis.
  • In plants, primary stem cells are located in shoot and root apical meristems (SAM and RAM) and secondary growth is ensured by cambium activation.
  • Besides the conservation of microtubules (MTs) and actin filaments (MFs), required for successful karyokinesis and cytokinesis, respectively, in all eukaryotes, plant mitotic cells present an original cytoskeleton organisation.
  • All the somatic cells of vascular plants lack centrosomes, and microtubule organising centres are spread all over the nuclear envelope, at the cell cortex and along pre‐existing microtubules.
  • Preceding the mitotic step per se, maintenance of centromere/kinetochore cohesion and integrity is required for the building of a bipolar spindle and accurate chromosome segregation.
  • During mitosis, the activity of MT nucleating complexes (TuRCs) and MT‐associated proteins (MAPs) leads to a succession of MT arrays that reorganise in the cytoplasm: cortical MTs/perinuclear MTs/pre‐prophase band MTs/spindle MTs/phragmoplast MTs. The spindle apparatus, consisting of kinetochore fibres and interpolar MTs, is barrel‐shaped and lacks polar asters. Some of the MAPs also connect MFs.
  • Gamma‐tubulin containing complexes and augmin complexes participate in the nucleation of new highly dynamic MTs that ensure spindle robustness.
  • Actin filaments intermingle with MTs and do not depolymerise during mitosis, except in the PPB, which becomes an actin‐deplete zone (ADZ).
  • The cell plate expands centrifugally to the cell edges thanks to actin filaments, preceding MTs on which Golgi‐derived vesicles move towards the equator and fuse together.

Keywords: plants; cell division; mitosis; cytoskeleton; microtubules; actin microfilaments; preprophase band; spindle; phragmoplast; centromere/kinetochore; centromere cohesion

Figure 1. Establishment of division polarity. Immunolabelling of MTs (red) and DAPI staining of chromatin (blue). (a, b) During G2 phase of the cell cycle, MTs are nucleated at the nuclear surface from dispersed γTuRC complexes. Then, they reorganise into small asters (arrows), which further converge to poles (arrow heads). They progressively form a bipolar prospindle. Simultaneously in the cortex, while polar cortical MTs depolymerise, a preprophase band formed by dense MT bundles (bracket) forecasts the location of the future cell plate. (c) z‐Stack of six views separated in the axis by 0.3 µm. (d) Details of an equatorial focal plane in the same prophase cell. Bars 2 µm.
Figure 2. MT dynamics throughout the cell cycle. (a) Immunolabelling of a root tip with anti‐tubulin antibodies, revealed using secondary antibodies marked by Alexa 568 fluorochrome. Chromatin staining using DAPI (blue). (b) Interphase cell with MTs radiating from the nuclear surface towards the cell cortex. (c) Early PPB and (d) mature PPB (brackets) in the cortex around the G2 nucleus. (e) Prophase cell with two polar caps and MT arrays pushing towards the nucleus. (f) Prometaphase spindle starting to spread at the poles. (g) Metaphase spindle with barrel‐shaped spindle poles. (h–j) Anaphase spindles refocalising the MT at poles through the activity of MAPs (e.g. ATK1). (k) Early telophase with phragmoplast MTs between daughter nuclei. (l) Late telophase with a wreath of short phragmoplast MTs growing centrifugically towards the cortex. Bars = 2 µm.
Figure 3. GIP1‐GFP expression under the control of its native promoter in mutant background. Chromosomes are labelled blue, using DAPI staining. GIP1 is a γTuRC component required for spindle robustness and genome maintenance. It localises on the spindle in metaphase (a), especially kinetochore fibres in anaphase (b) and relocates in telophase on the phragmoplast (c). Bars = 2 µm.
Figure 4. Phragmoplast MT immunolabelling in late telophase. (a–f) Six focal planes separated by 1 µm in the axis show the wreath‐like organisation of phragmoplast MTs. (a, c) Cell surface. Two sets of MTs, parallel to the spindle axis but with opposite polarity intermingle at the centre of the interzone. Their (+) end is located at the cell plate. (d–f) In a more central part of the cell where daughter nuclei become visible after DAPI staining (blue), the growing cell plate (dotted line in f) forms by Golgi‐derived vesicle fusion. MTs depolymerise in the central part of the cell and new MT assembly takes place at the periphery, allowing centrifugal extension and further fusion of the cell plate with the mother plasma membrane. Bars = 2 µm.
Figure 5. Schematic drawing of MT and MF dynamics throughout the cell cycle of plant cells. Proteins involved in each peculiar cytoskeletal array are mentioned on the sides.
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References

Ambrose JC, Tsubasa S, Kotzer AM, et al. (2007) The Arabidopsis CLASP gene encodes a microtubule‐associated protein involved in cell expansion and division. Plant Cell 19 (9): 2763–2775.

Azimzadeh J, Nacry P, Christodoulidou A, et al. (2008) Arabidopsis TONNEAU1 proteins are essential for preprophase band formation and interact with centrin. Plant Cell 20 (8): 2146–2159.

Boruc J, Van den Daele H, Hollunder J, et al. (2010) Functional modules in the Arabidopsis core cell cycle binary protein‐protein interaction network. Plant Cell 22 (4): 1264–1280.

Burian A, Ludynia M, Uyttewaal M, et al. (2013) A correlative microscopy approach relates microtubule behaviour, local organ geometry, and cell growth at the Arabidopsis shoot apical meristem. Journal of Experimental Botany 64 (18): 5753–5767.

Buschmann H, Chan J, Sanchez‐Pulido L, et al. (2006) Microtubule‐associated AIR9 recognizes the cortical division site at preprophase and cell‐plate insertion. Current Biology 16 (19): 1938–1943.

Camilleri C, Azimzadeh J, Pastuglia M, et al. (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 (4): 833–845.

Chabouté ME and Berr A (2016) GIP Contributions to the regulation of centromere at the interface between the nuclear envelope and the nucleoplasm. Frontiers in Plant Science 7: 118.

Clayton L and Lloyd CW (1985) Actin organization during the cell cycle in meristematic plant cells. Actin is present in the cytokinetic phragmoplast. Experimental Cell Research 156 (1): 231–238.

Cromer L, Jolivet S, Horlow C, et al. (2013) Centromeric cohesion is protected twice at meiosis, by SHUGOSHINs at anaphase I and by PATRONUS at interkinesis. Current Biology 23 (21): 2090–2099.

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. Proceedings of the National Academy of Sciences of the United States of America 79 (6): 1898–1902.

Deinum EE and Mulder BM (2013) Modelling the role of microtubules in plant cell morphology. Current Opinion in Plant Biology 16 (6): 688–692.

Drevensek S, Goussot M, Duroc Y, et al. (2012) The Arabidopsis TRM1‐TON1 interaction reveals a recruitment network common to plant cortical microtubule arrays and eukaryotic centrosomes. Plant Cell 24 (1): 178–191.

Gruss OJ, Wittmann M, Yikoyama H, et al. (2002) Chromosome‐induced microtubule assembly mediated by TPX2 is required for spindle formation in HeLa cells. Nature Cell Biology 4 (11): 871–879.

Hayashi T, Sano T, Kutsuna N, et al. (2007) Contribution of anaphase B to chromosome separation in higher plant cells estimated by image processing. Plant Cell Physiology 48 (10): 1509–1513.

Ho CM, Hotta T, Kong Z, et al. (2011) Augmin plays a critical role in organizing the spindle and phragmoplast microtubule arrays in Arabidopsis. Plant Cell 23 (7): 2606–2618.

Hutchins JR, Toyoda Y, Hegemann B, et al. (2010) Systematic analysis of human protein complexes identifies chromosome segregation proteins. Science 328 (5978): 593–599.

Janski N, Herzog E, Schmit AC, et al. (2008) Identification of a novel small Arabidopsis protein interacting with gamma‐tubulin complex protein 3. Cell Biology International 32 (5): 546–548.

Janski N, Masoud K, Batzenschlager M, et al. (2012) The GCP3‐interacting proteins GIP1 and GIP2 are required for gamma‐tubulin complex protein localization, spindle integrity, and chromosomal stability. Plant Cell 24 (3): 1171–1187.

Juraniec M, Heyman J, Schubert V, et al. (2015) Arabidopsis COPPER MODIFIED RESISTANCE1/PATRONUS1 is essential for growth adaptation to stress and required for mitotic onset control. New Phytologist 209 (1): 177–191.

Jurgens G, Park M, Richter S, et al. (2015) Plant cytokinesis: a tale of membrane traffic and fusion. Biochemical Society Transactions 43 (1): 73–78.

Karsenti E and Vernos I (2001) The mitotic spindle: a self‐made machine. Science 294 (5542): 543–547.

de Keijzer J, Mulder BM, Janson ME, et al. (2014) Microtubule networks for plant cell division. Systems and Synthetic Biology 8 (3): 187–194.

Klotz J and Nick P (2012) A novel actin‐microtubule cross‐linking kinesin, NtKCH, functions in cell expansion and division. New Phytologist 193 (3): 576–589.

Kojo KH, Higaki T, Kutsuna N, et al. (2013) Roles of cortical actin microfilament patterning in division plane orientation in plants. Plant Cell Physiology 54 (9): 1491–1503.

Kojo KH, Yasuhara H, Hasezawa S, et al. (2014) Time‐sequential observation of spindle and phragmoplast orientation in BY‐2 cells with altered cortical actin microfilament patterning. Plant Signaling and Behavior 9 (8): e29579.

Li S, Sun T, Ren H, et al. (2015) The functions of the cytoskeleton and associated proteins during mitosis and cytokinesis in plant cells. Frontiers in Plant Science 6: 282.

Lipka E, Gadeyne A, Stockle D, et al. (2014) The phragmoplast‐orienting kinesin‐12 class proteins translate the positional information of the preprophase band to establish the cortical division zone in Arabidopsis thaliana. Plant Cell 26 (6): 2617–2632.

Lloyd C and Chan J (2006) Not so divided: the common basis of plant and animal cell division. Nature Reviews in Molecular Cell Biology 7 (2): 147–152.

Malcos JL and Cyr RJ (2011) An ungrouped plant kinesin accumulates at the preprophase band in a cell cycle‐dependent manner. Cytoskeleton (Hoboken) 68 (4): 247–258.

Masuda H, Mori R, Yukawa M, et al. (2013) Fission yeast MOZART1/Mzt1 is an essential gamma‐tubulin complex component required for complex recruitment to the microtubule organizing center, but not its assembly. Molecular Biology of the Cell 24 (18): 2894–2906.

Mole‐Bajer J, Bajer AS, Inoue S, et al. (1988) Three‐dimensional localization and redistribution of F‐actin in higher plant mitosis and cell plate formation. Cell Motility and the Cytoskeleton 10 (1–2): 217–228.

Paganelli L, Caillaud MC, Quentin M, et al. (2015) Three BUB1 and BUBR1/MAD3‐related spindle assembly checkpoint proteins are required for accurate mitosis in Arabidopsis. New Phytologist 205 (1): 202–215.

Pastuglia M and Bouchez D (2007) Molecular encounters at microtubule ends in the plant cell cortex. Current Opinion in Plant Biology 10 (6): 557–563.

Petrovska B, Cenklova V, Pochylova Z, et al. (2012) Plant Aurora kinases play a role in maintenance of primary meristems and control of endoreduplication. New Phytologist 193 (3): 590–604.

Pietra S, Gustavsson A, Kiefer C, et al. (2013) Arabidopsis SABRE and CLASP interact to stabilize cell division plane orientation and planar polarity. Nature Communications 4: 2779.

Rybak K, Steiner A, Synek L, et al. (2014) Plant cytokinesis is orchestrated by the sequential action of the TRAPPII and exocyst tethering complexes. Developmental Cell 29 (5): 607–620.

Schmit AC, Vantard M, de Mey J, et al. (1983) Aster‐like microtubule centers establish spindle polarity during interphase – mitosis transition in higher plant cells. Plant Cell Reports 2 (6): 285–288.

Schmit AC and Lambert AM (1987) Characterization and dynamics of cytoplasmic F‐actin in higher plant endosperm cells during interphase, mitosis, and cytokinesis. Journal of Cell Biology 105 (5): 2157–2166.

Schmit AC and Lambert AM (1990) Microinjected fluorescent phalloidin in vivo reveals the F actin dynamics and assembly in higher plant mitotic cells. Plant Cell 2 (2): 129–138.

Spinner L, Gadeyne A, Belcram K, et al. (2013) A protein phosphatase 2A complex spatially controls plant cell division. Nature Communications 4: 1863.

Steiner A, Muller L, Rybak K, et al. (2015) The membrane‐associated Sec1/Munc18 KEULE is required for phragmoplast microtubule reorganization during cytokinesis in Arabidopsis. Molecular Plant. DOI: 10.1016/j.molp.2015.12.005.

Traas JA, Doonan JH, Rawlins DJ, et al. (1987) An actin network is present in the cytoplasm throughout the cell cycle of carrot cells and associates with the dividing nucleus. Journal of Cell Biology 105 (1): 387–395.

Van Damme D, Vanstraelen M, Geelen D, et al. (2007) Cortical division zone establishment in plant cells. Trends in Plant Sciences 12 (10): 458–464.

Van Damme D, Gadeyne A, Vanstraelen M, et al. (2011) Adaptin‐like protein TPLATE and clathrin recruitment during plant somatic cytokinesis occurs via two distinct pathways. Proceedings of the National Academy of Sciences of the United States of America 108 (2): 615–620.

Van Leene J, Stals H, Eeckhout D, et al. (2007) A tandem affinity purification‐based technology platform to study the cell cycle interactome in Arabidopsis thaliana. Molecular & Cellular Proteomics 6 (7): 1226–1238.

Voigt B, Timmers AC, Samaj J, et al. (2005) GFP‐FABD2 fusion construct allows in vivo visualization of the dynamic actin cytoskeleton in all cells of Arabidopsis seedlings. European Journal of Cell Biology 84 (6): 595–608.

Vos JW, Pieuchot L, Evrard JL, et al. (2008) The plant TPX2 protein regulates prospindle assembly before nuclear envelope breakdown. Plant Cell 20 (10): 2783–2797.

Walker KL, Muller S, Moss D, et al. (2007) Arabidopsis TANGLED 1 identifies the division plane throughout mitosis and cytokinesis. Current Biology 17 (21): 1827–1836.

Wright AJ, Gallagher K, Smith LG, et al. (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 (1): 234–247.

Wu SZ and Bezanilla M (2014) Myosin VIII associates with microtubule ends and together with actin plays a role in guiding plant cell division. Elife 3. DOI: 10.7554/eLife.03498.

Further Reading

Batzenschlager M, Lermontova I, Schubert V, et al. (2015) Arabidopsis MZT1 homologs GIP1 and GIP2 are essential for centromere architecture. Proceedings of the National Academy of Sciences of the United States of America 112 (28): 8656–8660.

Bouchez D, Van Damme D, Boruc J, et al. (2014) Cell division plane determination in plant development. In: Sarah Assmann and Bo Liu (eds) Cell Biology. New York: Springer Science + Business Media New York. DOI: 10.1007/978-1-4614-7881-2_15-1.

Li S, Sun T, Ren H, et al. (2015) The functions of the cytoskeleton and associated proteins during mitosis and cytokinesis in plant cells. Frontiers in Plant Science 6: 282.

Lipka E, Herrmann A and Mueller S (2015) Mechanisms of plant cell division. WIREs Developmental Biology 4: 391–405. DOI: 10.1002/wdev.186.

Rasmussen CG, Wright AJ and Müller S (2013) The role of the cytoskeleton and associated proteins in determination of the plant cell division plane. Plant Journal 75 (2): 258–269.

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Chabouté, Marie‐Edith, and Schmit, Anne‐Catherine(Jul 2016) Unique Characteristics of Cell Division in Vascular Plants. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0001686.pub3]