Division plane determination during plant somatic cytokinesis

Current Opinion in Plant Biology

Volumn 12, Issue 6, 2009, Pages 745-751

  Van Damme, Daniel ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

VEGETABLE PROTEIN;

CYTOKINESIS; CYTOLOGY; METABOLISM; MITOSIS SPINDLE; PLANT; REVIEW;

CYTOKINESIS; MITOTIC SPINDLE APPARATUS; PLANT PROTEINS; PLANTS;

EID: 70450203677     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2009.09.014     Document Type: Review

References (56)

1. Oliferenko S., Chew T.G., and Balasubramanian M.K. Positioning cytokinesis. Genes Dev 23 (2009) 660-674. The above review provides an excellent overview and compares the different modes of division plane positioning and the execution of cytokinesis in yeast, animal, and plant cells. As it mainly focuses on the latest findings and current biological questions regarding animal and yeast cytokinesis, it provides an excellent opportunity for plant biologists to keep up with the progress in other fields.
2. Ambrose J.C., Shoji T., Kotzer A.M., Pighin J.A., and Wasteneys G.O. The Arabidopsis CLASP gene encodes a microtubule-associated protein involved in cell expansion and division. Plant Cell 19 (2007) 2763-2775
3. Dhonukshe P., and Gadella Jr. T.W. Alteration of microtubule dynamic instability during preprophase band formation revealed by yellow fluorescent protein-CLIP170 microtubule plus-end labeling. Plant Cell 15 (2003) 597-611
4. Gaillard J., Neumann E., Van Damme D., Stoppin-Mellet V., Ebel C., Barbier E., Geelen D., and Vantard M. Two microtubule-associated proteins of Arabidopsis MAP65s promote antiparallel microtubule bundling. Mol Biol Cell 19 (2008) 4534-4544. This work describes the molecular properties of two members of the MAP65 protein family and for the first time shows the intrinsic capacity of these plant proteins to bundle antiparallel microtubules. Furthermore, clear evidence is provided that Arabidopsis MAP65-1 and MAP65-5 proteins are differentially regulated. This is concluded from the fact that they show different affinities for the various microtubular arrays throughout cell division. The localization data furthermore confirms previous observations that cortical and PPB microtubule properties are regulated independently from the mitotic ones.
5. Kawamura E., Himmelspach R., Rashbrooke M.C., Whittington A.T., Gale K.R., Collings D.A., and Wasteneys G.O. MICROTUBULE ORGANIZATION 1 regulates structure and function of microtubule arrays during mitosis and cytokinesis in the Arabidopsis root. Plant Physiol 140 (2006) 102-114
6. Kirik V., Herrmann U., Parupalli C., Sedbrook J.C., Ehrhardt D.W., and Hulskamp M. CLASP localizes in two discrete patterns on cortical microtubules and is required for cell morphogenesis and cell division in Arabidopsis. J Cell Sci 120 (2007) 4416-4425
7. Vos J.W., Dogterom M., and Emons A.M. Microtubules become more dynamic but not shorter during preprophase band formation: a possible "search-and-capture" mechanism for microtubule translocation. Cell Motil Cytoskeleton 57 (2004) 246-258
8. Ayaydin F., Vissi E., Meszaros T., Miskolczi P., Kovacs I., Feher A., Dombradi V., Erdodi F., Gergely P., and Dudits D. 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 (2000) 85-96
9. Nogami A., and Mineyuki Y. Loosening of a preprophase band of microtubules in onion (Allium cepa L.) root tip cells by kinase inhibitors. Cell Struct Funct 24 (1999) 419-424
10. Tian G.W., Smith D., Gluck S., and Baskin T.I. Higher plant cortical microtubule array analyzed in vitro in the presence of the cell wall. Cell Motil Cytoskeleton 57 (2004) 26-36
11. Azimzadeh J., Nacry P., Christodoulidou A., Drevensek S., Camilleri C., Amiour N., Parcy F., Pastuglia M., and Bouchez D. Arabidopsis TONNEAU1 proteins are essential for preprophase band formation and interact with centrin. Plant Cell 20 (2008) 2146-2159. This paper describes the TON1 locus in Arabidopsis and its specific involvement in cortical microtubule organization, required for anisotropic growth and preprophase band formation. TON1 proteins are conserved among land plants and share homology with animal centrosomal proteins. The punctuate localization of GFP-TON1 and its association with Arabidopsis CENTRIN point to TON1 as part of cortical microtubule-nucleation centers consistent with the plant cell cortex acting as a flexible centrosome.
12. Camilleri C., Azimzadeh J., Pastuglia M., Bellini C., Grandjean O., and 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 14 (2002) 833-845
13. Wright A.J., Gallagher K., and Smith L.G. 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 (2009) 234-247. This study describes the molecular characterization of the maize homologs of Arabidopsis FASS. Both DCD1 and ADD1 are highly homologous proteins that function redundantly in PPB formation and are essential to orient symmetrical and asymmetrical divisions in maize leaves, although DCD1 appears to have a more pronounced function in asymmetrical divisions than ADD1. They also show that DCD1 and ADD1 remain localized at the cortical division zone after PPB degradation, at least until metaphase, which suggests for the first time that the function of the FASS-containing PP2A complex in division plane positioning extends beyond PPB formation.
14. Goldberg Y. Protein phosphatase 2A: who shall regulate the regulator?. Biochem Pharmacol 57 (1999) 321-328
15. Benschop J.J., Mohammed S., O'Flaherty M., Heck A.J., Slijper M., and Menke F.L. Quantitative phosphoproteomics of early elicitor signaling in Arabidopsis. Mol Cell Proteomics 6 (2007) 1198-1214. This paper reports on a mass spectrometry-based quantitative phosphoproteomics approach of plasma membrane-associated proteins in Arabidopsis. The scope of the paper is to identify differential phosphorylation of signaling and response proteins leading to early defense response. Next to this, by identifying specific phosphorylated residues of various plasma membrane-associated proteins, the paper also contains a wealth of information relevant for general plant cell biological research of plasma membrane proteins and their phosphorylated residues.
16. Sugiyama N., Nakagami H., Mochida K., Daudi A., Tomita M., Shirasu K., and Ishihama Y. Large-scale phosphorylation mapping reveals the extent of tyrosine phosphorylation in Arabidopsis. Mol Syst Biol 4 (2008) 193
17. Demidov D., Van Damme D., Geelen D., Blattner F.R., and Houben A. Identification and dynamics of two classes of aurora-like kinases in Arabidopsis and other plants. Plant Cell 17 (2005) 836-848
18. Van Leene J., Stals H., Eeckhout D., Persiau G., Van De Slijke E., Van Isterdael G., De Clercq A., Bonnet E., Laukens K., Remmerie N., et al. A tandem affinity purification-based technology platform to study the cell cycle interactome in Arabidopsis thaliana. Mol Cell Proteomics 6 (2007) 1226-1238
19. Weingartner M., Binarova P., Drykova D., Schweighofer A., David J.P., Heberle-Bors E., Doonan J., and Bogre L. Dynamic recruitment of Cdc2 to specific microtubule structures during mitosis. Plant Cell 13 (2001) 1929-1943
20. Michniewicz M., Zago M.K., Abas L., Weijers D., Schweighofer A., Meskiene I., Heisler M.G., Ohno C., Zhang J., Huang F., et al. Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell 130 (2007) 1044-1056. This work identifies the Protein Phosphatase 2A complex as an antagonistic regulator of the PINOID kinase in PIN phosphorylation, which mediates the apical-basal targeting of these proteins. This post-translational mechanism allows fast modulation of the direction of intercellular auxin fluxes, essential to regulate differential growth, tissue patterning, and organogenesis.
21. Blakeslee J.J., Zhou H.W., Heath J.T., Skottke K.R., Barrios J.A., Liu S.Y., and DeLong A. Specificity of RCN1-mediated protein phosphatase 2A regulation in meristem organization and stress response in roots. Plant Physiol 146 (2008) 539-553
22. Boutte Y., Crosnier M.T., Carraro N., Traas J., and Satiat-Jeunemaitre B. The plasma membrane recycling pathway and cell polarity in plants: studies on PIN proteins. J Cell Sci 119 (2006) 1255-1265
23. Dhonukshe P., Mathur J., Hulskamp M., and Gadella Jr. T.W. Microtubule plus-ends reveal essential links between intracellular polarization and localized modulation of endocytosis during division-plane establishment in plant cells. BMC Biol 3 (2005) 11
24. Mineyuki Y. The preprophase band of microtubules: its function as a cytokinetic apparatus in higher plants. Int Rev Cytol: Surv Cell Biol 187 (1999) 1-49
25. Chan J., Calder G., Fox S., and Lloyd C. Localization of the microtubule end binding protein EB1 reveals alternative pathways of spindle development in Arabidopsis suspension cells. Plant Cell 17 (2005) 1737-1748
26. Doonan J.H., Cove D.J., and Lloyd C.W. Immunofluorescence microscopy of microtubules in intact cell lineages of the moss, Physcomitrella patens. I. Normal and CIPC-treated tip cells. J Cell Sci 75 (1985) 131-147
27. Granger C.L., and Cyr R.J. Microtubule reorganization in tobacco BY-2 cells stably expressing GFP-MBD. Planta 210 (2000) 502-509
28. Panteris E., Apostolakos P., and Galatis B. 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 (2006) 696-709
29. Yoneda A., Akatsuka M., Hoshino H., Kumagai F., and Hasezawa S. Decision of spindle poles and division plane by double preprophase bands in a BY-2 cell line expressing GFP-tubulin. Plant Cell Physiol 46 (2005) 531-538
30. Krupnova T., Sasabe M., Ghebreghiorghis L., Gruber C.W., Hamada T., Dehmel V., Strompen G., Stierhof Y.D., Lukowitz W., Kemmerling B., et al. Microtubule-associated kinase-like protein RUNKEL needed for cell plate expansion in Arabidopsis cytokinesis. Curr Biol 19 (2009) 518-523. This study describes a novel cell cycle regulated microtubule-binding protein with a role in phragmoplast organization and cell plate expansion. Degradation of RUNKEL following metaphase by attaching a Dbox sequence does not rescue the mutant phenotype, demonstrating its requirement during cytokinesis. RUNKEL associates with all mitotic microtubular arrays, but does not associate with interphase cortical microtubules, confirming the hypothesis that the mitotic microtubule arrays recruit different sets of MAPs.
31. Van Damme D., Van Poucke K., Boutant E., Ritzenthaler C., Inze D., and Geelen D. In vivo dynamics and differential microtubule-binding activities of MAP65 proteins. Plant Physiol 136 (2004) 3956-3967
32. •]. Together, this points to a function for the POK kinesins as anchor proteins for CDZ identity markers.
33. Ciciarello M., Mangiacasale R., and Lavia P. Spatial control of mitosis by the GTPase Ran. Cell Mol Life Sci 64 (2007) 1891-1914
34. Vos J.W., Pieuchot L., Evrard J.L., Janski N., Bergdoll M., de Ronde D., Perez L.H., Sardon T., Vernos I., and Schmit A.C. The plant TPX2 protein regulates prospindle assembly before nuclear envelope breakdown. Plant Cell 20 (2008) 2783-2797. This work provides evidence that the Arabidopsis TPX2 homolog functions in prospindle assembly and they show by computational modeling that it is likely to interact with Arabidopsis Aurora 1 and 2, and less likely with Aurora 3, which is in agreement with the published localization data on these proteins [17,36]. Moreover, they were able to show that TPX2 binds Xenopus importin alpha and that this interaction is abolished by RanGTP. These results hint to the possibility that, analogous to animal systems, RanGTP-dependent release of TPX2 from importins in Arabidopsis could lead to subsequent activation of Arabidopsis Aurora kinases and bipolar spindle establishment.
35. Sardon T., Peset I., Petrova B., and Vernos I. Dissecting the role of Aurora A during spindle assembly. EMBO J 27 (2008) 2567-2579
36. Kawabe A., Matsunaga S., Nakagawa K., Kurihara D., Yoneda A., Hasezawa S., Uchiyama S., and Fukui K. Characterization of plant Aurora kinases during mitosis. Plant Mol Biol 58 (2005) 1-13
37. Eckerdt F., Eyers P.A., Lewellyn A.L., Prigent C., and Maller J.L. Spindle pole regulation by a discrete Eg5-interacting domain in TPX2. Curr Biol 18 (2008) 519-525
38. Bannigan A., Scheible W.R., Lukowitz W., Fagerstrom C., Wadsworth P., Somerville C., and Baskin T.I. A conserved role for kinesin-5 in plant mitosis. J Cell Sci 120 (2007) 2819-2827
39. Marcus A.I., Dixit R., and Cyr R.J. Narrowing of the preprophase microtubule band is not required for cell division plane determination in cultured plant cells. Protoplasma 226 (2005) 169-174
40. Sano T., Higaki T., Oda Y., Hayashi T., and Hasezawa S. 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 (2005) 595-605
41. Panteris E. Cortical actin filaments at the division site of mitotic plant cells: a reconsideration of the 'actin-depleted zone'. New Phytol 179 (2008) 334-341
42. Vanstraelen M., Van Damme D., De Rycke R., Mylle E., Inze D., and Geelen D. Cell cycle-dependent targeting of a kinesin at the plasma membrane demarcates the division site in plant cells. Curr Biol 16 (2006) 308-314
43. Karahara I., Suda J., Tahara H., Yokota E., Shimmen T., Misaki K., Yonemura S., Staehelin L.A., and Mineyuki Y. The preprophase band is a localized center of clathrin-mediated endocytosis in late prophase cells of the onion cotyledon epidermis. Plant J 57 (2009) 819-831. This paper uses electron tomography of epidermal onion cells to compare the abundance of clathrin-coated pits and vesicles inside and outside the PPB region. Quantitative analysis shows a higher abundance of clathrin-coated pits and vesicles at the PPB, while no differences in secretory activity could be detected. This work nicely confirms previous observations of enhanced endocytotic activity at the plasma membrane occupied by the preprophase band [23].
44. •], its maintenance at the CDZ following PPB degradation is microtubule-independent but requires both POK kinesins. Following PPB degradation, AtTAN localizes at the CDZ as a broad ring that narrows down during the later phases of cytokinesis, indicating the presence of a yet unknown level of control in division zone establishment that restricts the division plane from a broad CDZ to the exact cell plate insertion site.
45. Smith L.G., Gerttula S.M., Han S., and Levy J. Tangled1: a microtubule binding protein required for the spatial control of cytokinesis in maize. J Cell Biol 152 (2001) 231-236
46. Muller S., Han S., and Smith L.G. Two kinesins are involved in the spatial control of cytokinesis in Arabidopsis thaliana. Curr Biol 16 (2006) 888-894
47. Hasezawa S., Sano T., and Nagata T. Oblique cell plate formation in tobacco BY-2 cells originates in double preprophase bands. J Plant Res 107 (1994) 355-359
48. Van Damme D., and Geelen D. Demarcation of the cortical division zone in dividing plant cells. Cell Biol Int 32 (2008) 178-187
49. Cannon M.C., Terneus K., Hall Q., Tan L., Wang Y., Wegenhart B.L., Chen L., Lamport D.T., Chen Y., and Kieliszewski M.J. Self-assembly of the plant cell wall requires an extensin scaffold. Proc Natl Acad Sci U S A 105 (2008) 2226-2231
50. Samuels A.L., Giddings Jr. T.H., and Staehelin L.A. Cytokinesis in tobacco BY-2 and root tip cells: a new model of cell plate formation in higher plants. J Cell Biol 130 (1995) 1345-1357
51. Thiele K., Wanner G., Kindzierski V., Jurgens G., Mayer U., Pachl F., and Assaad F.F. The timely deposition of callose is essential for cytokinesis in Arabidopsis. Plant J 58 (2009) 16-23
52. Van Damme D., Coutuer S., De Rycke R., Bouget F.Y., Inze D., and Geelen D. Somatic cytokinesis and pollen maturation in Arabidopsis depend on TPLATE, which has domains similar to coat proteins. Plant Cell 18 (2006) 3502-3518
53. Buschmann H., Chan J., Sanchez-Pulido L., Andrade-Navarro M.A., Doonan J.H., and Lloyd C.W. Microtubule-associated AIR9 recognizes the cortical division site at preprophase and cell-plate insertion. Curr Biol 16 (2006) 1938-1943
54. Van Damme D., Bouget F.Y., Van Poucke K., Inze D., and Geelen D. Molecular dissection of plant cytokinesis and phragmoplast structure: a survey of GFP-tagged proteins. Plant J 40 (2004) 386-398
55. Mineyuki Y., and Gunning B.E.S. A role for preprophase bands of microtubules in maturation of cell-walls, and a general proposal on the function of preprophase band sites in cell-division in higher-plants. J Cell Sci 97 (1990) 527-537
56. Casimiro I., Beeckman T., Graham N., Bhalerao R., Zhang H., Casero P., Sandberg G., and Bennett M.J. Dissecting Arabidopsis lateral root development. Trends Plant Sci 8 (2003) 165-171