Universal rules for division plane selection in plants

Protoplasma

Volumn 249, Issue 2, 2012, Pages 239-253

  Müller, Sabine ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Actin filaments; Cell division; Cell shape; Cytoskeleton; Division plane orientation; Microtubules; Phragmoplast; Preprophase band

Indexed keywords

CELL DIVISION; CELL SHAPE; CYTOSKELETON; METABOLISM; MICROTUBULE; PHYSIOLOGY; PLANT CELL; REVIEW;

CELL DIVISION; CELL SHAPE; CYTOSKELETON; MICROTUBULES; PLANT CELLS;

EID: 84858341249     PISSN: 0033183X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00709-011-0289-y     Document Type: Review

References (116)

1. Almonacid M, Moseley JB, Janvore J, Mayeux A, Fraisier V, Nurse P, Paoletti A (2009) Spatial control of cytokinesis by Cdr2 kinase and Mid1/anillin nuclear export. Curr Biol 19: 961-966.
2. Ambrose JC, Shoji T, Kotzer AM, Pighin JA, Wasteneys GO (2007) The Arabidopsis CLASP gene encodes a microtubule-associated protein involved in cell expansion and division. Plant Cell Online 19: 2763-2775.
3. 14C]tyrosine by brain extract. Separation of a carboxypeptidase from tubulin-tyrosine ligase. Mol Cell Biochem 19: 17-21.
4. Azimzadeh J, Nacry P, Christodoulidou A, Drevensek S, Camilleri C, Amiour N, Parcy F, Pastuglia M, Bouchez D (2008) Arabidopsis TONNEAU1 proteins are essential for preprophase band formation and interact with centrin. Plant Cell 20: 2146-2159.
5. Bement WM, Benink HA, von Dassow G (2005) A microtubule-dependent zone of active RhoA during cleavage plane specification. J Cell Biol 170: 91-101.
6. Besson S, Dumais J (2011) Universal rule for the symmetric division of plant cells. Proc Natl Acad Sci. doi: 10. 1073/pnas. 1011866108.
7. Bisgrove SR, Hable WE, Kropf DL (2004) +TIPs and microtubule regulation. The beginning of the plus end in plants. Plant Physiol 136: 3855-3863.
8. Bisgrove SR, Lee YR, Liu B, Peters NT, Kropf DL (2008) The microtubule plus-end binding protein EB1 functions in root responses to touch and gravity signals in Arabidopsis. Plant Cell 20: 396-410.
9. Boruc J, Mylle E, Duda M, De Clercq R, Rombauts S, Geelen D, Hilson P, Inze D, van Damme D, Russinova E (2010) Systematic localization of the Arabidopsis core cell cycle proteins reveals novel cell division complexes. Plant Physiol 152: 553-565.
10. Boutte Y, Frescatada-Rosa M, Men S, Chow CM, Ebine K, Gustavsson A, Johansson L, Ueda T, Moore I, Jürgens G, Grebe M (2010) Endocytosis restricts Arabidopsis KNOLLE syntaxin to the cell division plane during late cytokinesis. EMBO J 29: 546-558.
11. Brown RC, Lemmon B, Nguyen H (2002) The microtubule cycle during successive mitotic waves in the syncytial female gametophyte of ginkgo. J Plant Res 115: 491-494.
12. Buschmann H, Chan J, Sanchez-Pulido L, Andrade-Navarro MA, Doonan JH, Lloyd CW (2006) Microtubule-associated AIR9 recognizes the cortical division site at preprophase and cell-plate insertion. Curr Biol 16: 1938-1943.
13. Bush SM, Krysan PJ (2007) Mutational evidence that the Arabidopsis MAP kinase MPK6 is involved in anther, inflorescence, and embryo development. J Exp Bot 58: 2181-2191.
14. Camilleri C, Azimzadeh J, Pastuglia M, Bellini C, Grandjean O, Bouchez D (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: 833-845.
15. Canman JC, Cameron LA, Maddox PS, Straight A, Tirnauer JS, Mitchison TJ, Fang G, Kapoor TM, Salmon ED (2003) Determining the position of the cell division plane. Nature 424: 1074-1078.
16. Chan J, Calder G, Fox S, Lloyd C (2005) Localization of the microtubule end binding protein EB1 reveals alternative pathways of spindle development in Arabidopsis suspension cells. Plant Cell 17: 1737-1748.
17. Chang F, Martin SG (2009) Shaping fission yeast with microtubules. Cold Spring Harb Perspect Biol 1: a001347.
18. Ciciarello M, Mangiacasale R, Lavia P (2007) Spatial control of mitosis by the GTPase Ran. Cell Mol Life Sci 64: 1891-1914.
19. 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.
20. 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.
21. Daga RR, Chang F (2005) Dynamic positioning of the fission yeast cell division plane. Proc Natl Acad Sci USA 102: 8228-8232.
22. Daga RR, Yonetani A, Chang F (2006) Asymmetric microtubule pushing forces in nuclear centering. Curr boil 16: 1544-1550.
23. De Smet I, Beeckman T (2011) Asymmetric cell division in land plants and algae: the driving force for differentiation. Nat Rev Mol Cell Biol 12: 177-188.
24. Dhonukshe P, Gadella TW Jr (2003) Alteration of microtubule dynamic instability during preprophase band formation revealed by yellow fluorescent protein-CLIP170 microtubule plus-end labeling. Plant Cell 15: 597-611.
25. Dhonukshe P, Mathur J, Hulskamp M, Gadella TW Jr (2005) Microtubule plus-ends reveal essential links between intracellular polarization and localized modulation of endocytosis during division-plane establishment in plant cells. BMC Biol 3: 11.
26. Dixit R, Cyr R (2002) Golgi secretion is not required for marking the preprophase band site in cultured tobacco cells. Plant J 29: 99-108.
27. Doonan JH, Cove DJ, Lloyd CW (1985) Immunofluorescence microscopy of microtubules in intact cell lineages of the moss. Physcomitrella patens. I. Normal and CIPC-treated tip cells. J Cell Sci 75: 131-147.
28. Dupuy L, Mackenzie J, Haseloff J (2010) Coordination of plant cell division and expansion in a simple morphogenetic system. Proc Natl Acad Sci 107: 2711-2716.
29. Ehrhardt DW, Shaw SL (2006) Microtubule dynamics and organization in the plant cortical array. Annu Rev Plant Biol 57: 859-875.
30. Errera L (1888) Über Zellformen und Seifeblasen. Bot Centralbl 34: 395-398.
31. Flanders DJ, Rawlins DJ, Shaw PJ, Lloyd CW (1990) 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 110: 1111-1122.
32. Gibson WT, Veldhuis JH, Rubinstein B, Cartwright HN, Perrimon N, Brodland GW, Nagpal R, Gibson MC (2011) Control of the mitotic cleavage plane by local epithelial topology. Cell 144: 427-438.
33. Glotzer M (2009) Cytokinesis: GAP gap. Curr Biol 19: R162-R165.
34. Goodbody KC, Venverloo CJ, Lloyd CW (1991) Laser microsurgery demonstrates that cytoplasmic strands anchoring the nucleus across the vacuole of premitotic plant cells are under tension. Implications for division plane alignment. Development 113: 931-939.
35. Gunning BES, Wick SM (1985) Preprophase bands, phragmoplasts, and spatial control of cytokinesis. J Cell Sci Suppl 2: 157-179.
36. Gutierrez R, Grossmann G, Frommer WB, Ehrhardt DW (2010) Opportunities to explore plant membrane organization with super-resolution microscopy. Plant Physiol 154: 463-466.
37. Hamann T, Benkova E, Baurle I, Kientz M, Jürgens G (2002) The Arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo patterning. Genes Dev 16: 1610-1615.
38. Hamant O, Heisler MG, Jönsson H, Krupinski P, Uyttewaal M, Bokov P, Corson F, Sahlin P, Boudaoud A, Meyerowitz EM, Couder Y, Traas J (2008) Developmental patterning by mechanical signals in Arabidopsis. Science 322: 1650-1655.
39. Hertwig O (1884) Das Problem der Befruchtung und der Isotropie des Eies, eine Theorie der Vererbung (Jenaische Zeitschrift der Naturwissenschaften).
40. Hetzer M, Bilbao-Cortes D, Walther TC, Gruss OJ, Mattaj IW (2000) GTP hydrolysis by Ran is required for nuclear envelope assembly. Mol Cell 5: 1013-1024.
41. Hoshino H, Yoneda A, Kumagai F, Hasezawa S (2003) 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 222: 157-165.
42. Idriss HT (2004) Three steps to cancer: how phosphorylation of tubulin, tubulin tyrosine ligase and P-glycoprotein may generate and sustain cancer. Cancer Chemother Pharmacol 54: 101-104.
43. Iwase M, Luo J, Nagaraj S, Longtine M, Kim HB, Haarer BK, Caruso C, Tong Z, Pringle JR, Bi E (2006) Role of a Cdc42p effector pathway in recruitment of the yeast septins to the presumptive bud site. Mol Biol Cell 17: 1110-1125.
44. Jovanović AM, Durst S, Nick P (2010) Plant cell division is specifically affected by nitrotyrosine. J Exp Bot 61: 901-909.
45. Jürgens G (2005) Cytokinesis in higher plants. Annu Rev Plant Biol 56: 281-299.
46. Karahara I, Suda J, Tahara H, Yokota E, Shimmen T, Misaki K, Yonemura S, Staehelin LA, Mineyuki Y (2009) The preprophase band is a localized center of clathrin-mediated endocytosis in late prophase cells of the onion cotyledon epidermis. Plant J 57: 819-831.
47. Kawamura E, Wasteneys GO (2008) MOR1, the Arabidopsis thaliana homologue of Xenopus MAP215, promotes rapid growth and shrinkage, and suppresses the pausing of microtubules in vivo. J Cell Sci 121: 4114-4123.
48. Kawamura E, Himmelspach R, Rashbrooke MC, Whittington AT, Gale KR, Collings DA, Wasteneys GO (2006) MICROTUBULE ORGANIZATION 1 regulates structure and function of microtubule arrays during mitosis and cytokinesis in the Arabidopsis root. Plant Physiol 140: 102-114.
49. Kirik V, Herrmann U, Parupalli C, Sedbrook JC, Ehrhardt DW, Hulskamp M (2007) CLASP localizes in two discrete patterns on cortical microtubules and is required for cell morphogenesis and cell division in Arabidopsis. J Cell Sci 120: 4416-4425.
50. Komaki S, Abe T, Coutuer S, Inze D, Russinova E, Hashimoto T (2010) Nuclear-localized subtype of end-binding 1 protein regulates spindle organization in Arabidopsis. J Cell Sci 123: 451-459.
51. Li H, Wu G, Ware D, Davis KR, Yang Z (1998) Arabidopsis Rho-related GTPases: differential gene expression in pollen and polar localization in fission yeast. Plant Physiol 118: 407-417.
52. Liao G, Gundersen GG (1998) Kinesin is a candidate for cross-bridging microtubules and intermediate filaments. J Biol Chem 273: 9797-9803.
53. 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.
54. Malcos JL, Cyr RJ (2011) An ungrouped plant kinesin accumulates at the preprophase band in a cell cycle-dependent manner. Cytoskeleton 68: 247-258.
55. Marcus AI, Dixit R, Cyr RJ (2005) Narrowing of the preprophase microtubule band is not required for cell division plane determination in cultured plant cells. Protoplasma 226: 169-174.
56. Martin SG (2009a) Geometric control of the cell cycle. Cell Cycle 8: 3643-3647.
57. Martin SG (2009b) Microtubule-dependent cell morphogenesis in the fission yeast. Trends Cell Biol 19: 447-454.
58. Meier I, Brkljacic J (2009) The nuclear pore and plant development. Curr Opin Plant Biol 12: 87-95.
59. Merkle T (2003) Nucleo-cytoplasmic partitioning of proteins in plants: implications for the regulation of environmental and developmental signalling. Curr Genet 44: 231-260.
60. Merkle T (2011) Nucleo-cytoplasmic transport of proteins and RNA in plants. Plant Cell Rep 30: 153-176.
61. Miller AL, Bement WM (2009) Regulation of cytokinesis by Rho GTPase flux. Nat Cell Biol 11: 71-77.
62. Minc N, Burgess D, Chang F (2011) Influence of cell geometry on division-plane positioning. Cell 144: 414-426.
63. Mineyuki Y (1999) The preprophase band of microtubules: its function as a cytokinetic apparatus in higher plants. In: Kwang WJ (ed) International review of cytology, vol 187. Academic Press, Burlington, pp 1-49.
64. 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.
65. 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.
66. Müller J, Beck M, Mettbach U, Komis G, Hause G, Menzel D, Samaj J (2010) Arabidopsis MPK6 is involved in cell division plane control during early root development, and localizes to the pre-prophase band, phragmoplast, trans-Golgi network and plasma membrane. Plant J 61: 234-248.
67. Murata T, Wada M (1991) Effects of centrifugation on preprophase-band formation in Adiantum protonemata. Planta 183: 391-398.
68. Nebenführ A, Frohlick JA, Staehelin LA (2000) Redistribution of Golgi stacks and other organelles during mitosis and cytokinesis in plant cells. Plant Physiol 124: 135-151.
69. Nguyen H, Brown RC, Lemmon BE (2002) Cytoskeletal organization of the micropylar endosperm in Coronopus didymus L. (Brassicaceae). Protoplasma 219: 210-220.
70. Nogami A, Mineyuki Y (1999) Loosening of a preprophase band of microtubules in onion (Allium cepa L.) root tip cells by kinase inhibitors. Cell Struct Funct 24: 419-424.
71. Odde D (2011) Getting cells and tissues into shape. Cell 144(3): 325-326.
72. Oliferenko S, Chew TG, Balasubramanian MK (2009) Positioning cytokinesis. Genes Dev 23: 660-674.
73. Otegui M, Staehelin LA (2000a) Cytokinesis in flowering plants: more than one way to divide a cell. Curr Opin Plant Biol 3: 493-502.
74. Otegui M, Staehelin LA (2000b) Syncytial-type cell plates: a novel kind of cell plate involved in endosperm cellularization of Arabidopsis. Plant Cell 12: 933-947.
75. Otegui MS, Verbrugghe KJ, Skop AR (2005) Midbodies and phragmoplasts: analogous structures involved in cytokinesis. Trends Cell Biol 15: 404-413.
76. Paciorek T, Bergmann DC (2010) The secret to life is being different: asymmetric divisions in plant development. Curr Opin Plant Biol 13: 661-669.
77. Panteris E (2008) Cortical actin filaments at the division site of mitotic plant cells: a reconsideration of the 'actin-depleted zone'. New Phytol 179: 334-341.
78. Pastuglia M, Bouchez D (2007) Molecular encounters at microtubule ends in the plant cell cortex. Curr Opin Plant Biol 10: 557-563.
79. Perrot-Rechenmann C (2010) Cellular responses to auxin: division versus expansion. Cold Spring Harb Perspect Biol 2: a001446.
80. Pickett-Heaps JD (1969) Preprophase microtubules and stomatal differentiation; some effects of centrifugation on symmetrical and asymmetrical cell division. J Ultrastruct Res 27: 24-44.
81. Prusinkiewicz P (2011) Inherent randomness of cell division patterns. Proc Natl Acad Sci 108: 5933-5934.
82. Rasmussen CG, Humphries JA, Smith LG (2011a) Determination of symmetric and asymmetric division planes in plant cells. Annu Rev Plant Biol 62: 387-409.
83. Rasmussen CG, Sun B, Smith LG (2011b) Tangled localization at the cortical division site of plant cells occurs by several mechanisms. J Cell Sci 124: 270-279.
84. Rodrigo-Peiris T, Xu XM, Zhao Q, Wang H-J, Meier I (2011) RanGAP is required for post-meiotic mitosis in female gametophyte development in Arabidopsis thaliana. J Exp Bot. doi: 10. 1093/jxb/erq448.
85. Sakai T, Honing HVD, Nishioka M, Uehara Y, Takahashi M, Fujisawa N, Saji K, Seki M, Shinozaki K, Jones MA, Smirnoff N, Okada K, Wasteneys GO (2008) Armadillo repeat-containing kinesins and a NIMA-related kinase are required for epidermal-cell morphogenesis in Arabidopsis. Plant J 53: 157-171.
86. Samaj J, Baluska F, Hirt H (2004) From signal to cell polarity: mitogen-activated protein kinases as sensors and effectors of cytoskeleton dynamicity. J Exp Bot 55: 189-198.
87. Sano T, Higaki T, Oda Y, Hayashi T, Hasezawa S (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.
88. Sasabe M, Soyano T, Takahashi Y, Sonobe S, Igarashi H, Itoh TJ, Hidaka M, Machida Y (2006) 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.
89. Sinott EW, Bloch R (1940) Cytoplasmic behavior during division of vacuolate plant cells. Proc Natl Acad Sci 26: 223-227.
90. Skoufias DA, Wilson L (1998) Assembly and colchicine binding characteristics of tubulin with maximally tyrosinated and detyrosinated [α]-tubulins. Arch Biochem Biophys 351: 115-122.
91. Smith LG, Gerttula SM, Han S, Levy J (2001) Tangled1: a microtubule binding protein required for the spatial control of cytokinesis in maize. J Cell Biol 152: 231-236.
92. Spinner L, Pastuglia M, Belcram K, Pegoraro M, Goussot M, Bouchez D, Schaefer DG (2010) The function of TONNEAU1 in moss reveals ancient mechanisms of division plane specification and cell elongation in land plants. Development 137: 2733-2742.
93. Suetsugu N, Yamada N, Kagawa T, Yonekura H, Uyeda TQP, Kadota A, Wada M (2010) Two kinesin-like proteins mediate actin-based chloroplast movement in Arabidopsis thaliana. Proc Natl Acad Sci 107: 8860-8865.
94. Takahashi Y, Soyano T, Sasabe M, Machida Y (2004) A MAP kinase cascade that controls plant cytokinesis. J Biochem 136: 127-132.
95. Thery M, Bornens M (2006) Cell shape and cell division. Curr Opin Cell Biol 18: 648-657.
96. Tirnauer JS, Salmon ED, Mitchison TJ (2004) Microtubule plus-end dynamics in Xenopus egg extract spindles. Mol Biol Cell 15: 1776-1784.
97. Tong Z, Gao X-D, Howell AS, Bose I, Lew DJ, Bi E (2007) Adjacent positioning of cellular structures enabled by a Cdc42 GTPase-activating protein-mediated zone of inhibition. J Cell Biol 179: 1375-1384.
98. Torres-Ruiz RA, Jürgens G (1994) Mutations in the FASS gene uncouple pattern formation and morphogenesis in Arabidopsis development. Development 120: 2967-2978.
99. Traas JA, Doonan JH, Rawlins DJ, Shaw PJ, Watts J, Lloyd CW (1987) An actin network is present in the cytoplasm throughout the cell cycle of carrot cells and associates with the dividing nucleus. J Cell Biol 105: 387-395.
100. Traas J, Bellini C, Nacry P, Kronenberger J, Bouchez D, Caboche M (1995) Normal differentiation patterns in plants lacking microtubular preprophase bands. Nature 375: 676-677.
101. van Damme D, Coutuer S, De Rycke R, Bouget FY, Inze D, Geelen D (2006) Somatic cytokinesis and pollen maturation in Arabidopsis depend on TPLATE, which has domains similar to coat proteins. Plant Cell 18: 3502-3518.
102. van Damme D, Gadeyne A, Vanstraelen M, Inze D, van Montagu MC, De Jaeger G, Russinova E, Geelen D (2011) Adaptin-like protein TPLATE and clathrin recruitment during plant somatic cytokinesis occurs via two distinct pathways. Proc Natl Acad Sci USA 108: 615-620.
103. 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, Henderickx K, De Vijlder T, Abdelkrim A, Pharazyn A, van Onckelen H, Inzé D, Witters E, De Jaeger G (2007) A tandem affinity purification-based technology platform to study the cell cycle interactome in Arabidopsis thaliana. Mol Cell Proteomics 6: 1226-1238.
104. Vanstraelen M, Torres Acosta JA, De Veylder L, Inze D, Geelen D (2004) A plant-specific subclass of C-terminal kinesins contains a conserved a-type cyclin-dependent kinase site implicated in folding and dimerization. Plant Physiol 135: 1417-1429.
105. Vanstraelen M, van Damme D, De Rycke R, Mylle E, Inze D, Geelen D (2006) Cell cycle-dependent targeting of a kinesin at the plasma membrane demarcates the division site in plant cells. Curr Biol 16: 308-314.
106. Vaughan KT (2005) TIP maker and TIP marker; EB1 as a master controller of microtubule plus ends. J Cell Biol 171: 197-200.
107. Verhey KJ, Hammond JW (2009) Traffic control: regulation of kinesin motors. Nat Rev Mol Cell Biol 10: 765-777.
108. von Dassow G (2009) Concurrent cues for cytokinetic furrow induction in animal cells. Trends Cell Biol 19: 165-173.
109. Vos JW, Dogterom M, Emons AM (2004) Microtubules 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.
110. Walker KL, Müller S, Moss D, Ehrhardt DW, Smith LG (2007) Arabidopsis TANGLED identifies the division plane throughout mitosis and cytokinesis. Curr Biol 17: 1827-1836.
111. Weingartner M, Binarova P, Drykova D, Schweighofer A, David J-P, Heberle-Bors E, Doonan J, Bögre L (2001) Dynamic recruitment of CDC2 to specific microtubule structures during mitosis. Plant Cell Online 13: 1929-1943.
112. Weingartner M, Criqui MC, Meszaros T, Binarova P, Schmit AC, Helfer A, Derevier A, Erhardt M, Bogre L, Genschik P (2004) Expression of a nondegradable cyclin B1 affects plant development and leads to endomitosis by inhibiting the formation of a phragmoplast. Plant Cell 16: 643-657.
113. Wolfe BA, Glotzer M (2009) Single cells (put a ring on it). Genes Dev 23: 896-901.
114. Wright AJ, Gallagher K, Smith LG (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: 234-247.
115. Xu XM, Zhao Q, Rodrigo-Peiris T, Brkljacic J, He CS, Müller S, Meier I (2008) RanGAP1 is a continuous marker of the Arabidopsis cell division plane. Proc Natl Acad Sci USA 105: 18637-18642.
116. Yang Z (2008) Cell polarity signaling in Arabidopsis. Annu Rev Cell Dev Biol 24: 551-575.