1932

Abstract

Plant cells divide their cytoplasmic content by forming a new membrane compartment, the cell plate, via a rerouting of the secretory pathway toward the division plane aided by a dynamic cytoskeletal apparatus known as the phragmoplast. The phragmoplast expands centrifugally and directs the cell plate to the preselected division site at the plasma membrane to fuse with the parental wall. The division site is transiently decorated by the cytoskeletal preprophase band in preprophase and prophase, whereas a number of proteins discovered over the last decade reside continuously at the division site and provide a lasting spatial reference for phragmoplast guidance. Recent studies of membrane fusion at the cell plate have revealed the contribution of functionally conserved eukaryotic proteins to distinct stages of cell plate biogenesis and emphasize the coupling of cell plate formation with phragmoplast expansion. Together with novel findings concerning preprophase band function and the setup of the division site, cytokinesis and its spatial control remain an open-ended field with outstanding and challenging questions to resolve.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-050718-100444
2019-04-29
2024-06-16
Loading full text...

Full text loading...

/deliver/fulltext/arplant/70/1/annurev-arplant-050718-100444.html?itemId=/content/journals/10.1146/annurev-arplant-050718-100444&mimeType=html&fmt=ahah

Literature Cited

  1. 1.  Abu-Abied M, Belausov E, Hagay S, Peremyslov V, Dolja V, Sadot E 2018. Myosin XI-K is involved in root organogenesis, polar auxin transport, and cell division. J. Exp. Bot. 69:2869–81
    [Google Scholar]
  2. 2.  Ahn G, Kim H, Kim DH, Hanh NH, Yoon Y et al. 2017. SH3P2 plays a crucial role at the step of membrane tubulation during cell plate formation in plants. Plant Cell 29:1388–405
    [Google Scholar]
  3. 3.  Ambrose C, Allard JF, Cytrynbaum EN, Wasteneys GO 2011. A CLASP-modulated cell edge barrier mechanism drives cell-wide cortical microtubule organization in Arabidopsis. Nat. Commun 2:430
    [Google Scholar]
  4. 4.  Ambrose JC, Cyr R 2008. Mitotic spindle organization by the preprophase band. Mol. Plant 1:950–60
    [Google Scholar]
  5. 5.  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 19:2763–75
    [Google Scholar]
  6. 6.  Apostolakos P, Galatis B 1992. Patterns of microtubule organization in 2 polyhedral cell-types in the gametophyte of the liverwort Marchantia paleacea Bert. New Phytol 122:165–78
    [Google Scholar]
  7. 7.  Apostolakos P, Livanos P, Giannoutsou E, Panteris E, Galatis B 2018. The intracellular and intercellular cross-talk during subsidiary cell formation in Zea mays: existing and novel components orchestrating cell polarization and asymmetric division. Ann. Bot. 122:679–96
    [Google Scholar]
  8. 8.  Arima K, Tamaoki D, Mineyuki Y, Yasuhara H, Nakai T et al. 2018. Displacement of the mitotic apparatuses by centrifugation reveals cortical actin organization during cytokinesis in cultured tobacco BY-2 cells. J. Plant Res. 131:803–15
    [Google Scholar]
  9. 9.  Austin JR, Seguí-Simarro JM, Staehelin LA 2005. Quantitative analysis of changes in spatial distribution and plus-end geometry of microtubules involved in plant-cell cytokinesis. J. Cell Sci. 118:3895–903
    [Google Scholar]
  10. 10.  Azimzadeh J, Nacry P, Christodoulidou A, Drevensek S, Camilleri C et al. 2008. Arabidopsis TONNEAU1 proteins are essential for preprophase band formation and interact with centrin. Plant Cell 20:2146–59
    [Google Scholar]
  11. 11.  Baluška F, Jasik J, Edelmann HG, Salajová T, Volkmann D 2001. Latrunculin B-induced plant dwarfism: plant cell elongation is F-actin-dependent. Dev. Biol. 231:113–24
    [Google Scholar]
  12. 12.  Bayer M, Slane D, Jürgens G 2017. Early plant embryogenesis—dark ages or dark matter. ? Curr. Opin. Plant Biol. 35:30–36
    [Google Scholar]
  13. 13.  Besson S, Dumais J 2011. Universal rule for the symmetric division of plant cells. PNAS 108:6294–99
    [Google Scholar]
  14. 14.  Bringmann M, Bergmann DC 2017. Tissue-wide mechanical forces influence the polarity of stomatal stem cells in Arabidopsis. Curr. Biol 27:877–83
    [Google Scholar]
  15. 15.  Bringmann M, Li E, Sampathkumar A, Kocabek T, Hauser MT, Persson S 2012. POM-POM2/CELLULOSE SYNTHASE INTERACTING1 is essential for the functional association of cellulose synthase and microtubules in Arabidopsis. Plant Cell 24:163–77
    [Google Scholar]
  16. 16.  Brown RC, Lemmon BE 2001. The cytoskeleton and spatial control of cytokinesis in the plant life cycle. Protoplasma 215:35–49
    [Google Scholar]
  17. 17.  Brown RC, Lemmon BE, Nguyen H 2002. The microtubule cycle during successive mitotic waves in the syncytial female gametophyte of ginkgo. J. Plant Res. 115:491–94
    [Google Scholar]
  18. 18.  Bürstenbinder K, Möller B, Plötner R, Stamm G, Hause G et al. 2017. The IQD family of calmodulin-binding proteins links calcium signaling to microtubules, membrane subdomains, and the nucleus. Plant Physiol 173:1692–708
    [Google Scholar]
  19. 19.  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. 16:1938–43
    [Google Scholar]
  20. 20.  Buschmann H, Dols J, Kopischke S, Peña EJ, Andrade-Navarro MA et al. 2015. Arabidopsis KCBP interacts with AIR9 but stays in the cortical division zone throughout mitosis via its MyTH4-FERM domain. J. Cell Sci. 128:2033–46
    [Google Scholar]
  21. 21.  Buschmann H, Holtmannspötter M, Borchers A, O'Donoghue MT, Zachgo S 2016. Microtubule dynamics of the centrosome‐like polar organizers from the basal land plant Marchantia polymorpha. New Phytol 209:999–1013
    [Google Scholar]
  22. 22.  Buschmann H, Zachgo S 2016. The evolution of cell division: from streptophyte algae to land plants. Trends Plant Sci 21:872–83
    [Google Scholar]
  23. 23.  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 14:833–45
    [Google Scholar]
  24. 24.  Chakrabortty B, Willemsen V, de Zeeuw T, Liao C-Y, Weijers D et al. 2018. A plausible microtubule-based mechanism for cell division orientation in plant embryogenesis. Curr. Biol. 28:3031–43.E2Utilizes computer simulations to predict division plane selection parameterizing cell geometry, microtubule dynamics, and auxin signaling.
    [Google Scholar]
  25. 25.  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 17:1737–48
    [Google Scholar]
  26. 26.  Chen H-W, Persson S, Grebe M, McFarlane HE Cellulose synthesis during cell plate assembly. Physiol. Plant. 164:17–26
    [Google Scholar]
  27. 27.  Chugh M, Reißner M, Bugiel M, Lipka E, Hermann A et al. 2018. Phragmoplast orienting kinesin 2 is a weak motor switching between processive and diffusive modes. Biophys. J. 115:375–85
    [Google Scholar]
  28. 28.  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 10:1875–88
    [Google Scholar]
  29. 29.  Craddock C, Lavagi I, Yang Z 2012. New insights into Rho signaling from plant ROP/Rac GTPases. Trends Cell Biol 22:492–501
    [Google Scholar]
  30. 30.  de Keijzer J, Kieft H, Ketelaar T, Goshima G, Janson ME 2017. Shortening of microtubule overlap regions defines membrane delivery sites during plant cytokinesis. Curr. Biol. 27:514–20Kinesin-4 in moss delimits the region of cell plate formation by regulating the length of antiparallel microtubules.
    [Google Scholar]
  31. 31.  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
    [Google Scholar]
  32. 32.  Ditengou FA, Teale WD, Kochersperger P, Flittner KA, Kneuper I et al. 2008. Mechanical induction of lateral root initiation in Arabidopsis thaliana. PNAS 105:18818–23
    [Google Scholar]
  33. 33.  Dong J, MacAlister CA, Bergmann DC 2009. BASL controls asymmetric cell division in Arabidopsis. Cell 137:1320–30
    [Google Scholar]
  34. 34.  Doty KF, Betzelberger AM, Kocot KM, Cook ME 2014. Immunofluorescence localization of the tubulin cytoskeleton during cell division and cell growth in members of the Coleochaetales (Streptophyta). J. Phycol. 50:624–39
    [Google Scholar]
  35. 35.  Drakakaki G 2015. Polysaccharide deposition during cytokinesis: challenges and future perspectives. Plant Sci 236:177–84
    [Google Scholar]
  36. 36.  Drevensek S, Goussot M, Duroc Y, Christodoulidou A, Steyaert S et al. 2012. The Arabidopsis TRM1–TON1 interaction reveals a recruitment network common to plant cortical microtubule arrays and eukaryotic centrosomes. Plant Cell 24:178–91
    [Google Scholar]
  37. 37.  Elliott A, Shaw SL 2018. Update: plant cortical microtubule arrays. Plant Physiol 176:94–105
    [Google Scholar]
  38. 38.  Fabien M, Thierry D, Eric B, Halima M, Katia B et al. 2014. Spatio-temporal analysis of cellulose synthesis during cell plate formation in Arabidopsis. Plant J 77:71–84
    [Google Scholar]
  39. 39.  Facette MR, Park Y, Sutimantanapi D, Luo A, Cartwright HN et al. 2015. The SCAR/WAVE complex polarizes PAN receptors and promotes division asymmetry in maize. Nat. Plants 1:14024
    [Google Scholar]
  40. 40.  Feng W, Kita D, Peaucelle A, Cartwright HN, Doan V et al. 2018. The FERONIA receptor kinase maintains cell-wall integrity during salt stress through Ca2+ signaling. Curr. Biol. 28:666–75
    [Google Scholar]
  41. 41.  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. 110:1111–22
    [Google Scholar]
  42. 42.  Galatis B, Apostolakos P, Katsaros C 1984. Positional inconsistency between preprophase microtubule band and final cell plate arrangement during subsidiary cell and hair cell formation in two Triticum species. Can. J. Bot. 62:342–59
    [Google Scholar]
  43. 43.  Galatis B, Mitrakos K 1979. On the differential divisions and preprophase microtubule bands involved in the development of stomata of Vigna sinensis L. J. Cell Sci. 37:11–37
    [Google Scholar]
  44. 44.  Giannoutsou E, Apostolakos P, Galatis B 2016. Spatio-temporal diversification of the cell wall matrix materials in the developing stomatal complexes of Zea mays. Planta 244:1125–43
    [Google Scholar]
  45. 45.  Gu F, Bringmann M, Combs JR, Yang J, Bergmann DC, Nielsen E 2016. Arabidopsis CSLD5 functions in cell plate formation in a cell cycle–dependent manner. Plant Cell 28:1722–37
    [Google Scholar]
  46. 46.  Hamant O 2017. Mechano-devo. Mech. Dev. 145:2–9
    [Google Scholar]
  47. 47.  Hamant O, Heisler MG, Jönsson H, Krupinski P, Uyttewaal M et al. 2008. Developmental patterning by mechanical signals in Arabidopsis. Science 322:1650–55
    [Google Scholar]
  48. 48.  Hepler PK 2016. The cytoskeleton and its regulation by calcium and protons. Plant Physiol 170:3–22
    [Google Scholar]
  49. 49.  Hepler PK, Jackson WT 1968. Microtubules and early stages of cell-plate formation in the endosperm of Haemanthus katherinae Baker. J. Cell Biol. 38:437–46
    [Google Scholar]
  50. 50.  Herrmann A, Livanos P, Lipka E, Gadeyne A, Hauser M-T et al. 2018. Dual localized kinesin-12 POK2 plays multiple roles during cell division and interacts with MAP65–3. EMBO Rep 19:e46085The dual localization of PHRAGMOPLAST-ORIENTING KINESIN 2 (POK2) during cytokinesis and its interaction with the midzone crosslinker MAP65–3 indicates functional diversification of plant kinesin-12.
    [Google Scholar]
  51. 51.  Hervieux N, Dumond M, Sapala A, Routier-Kierzkowska AL, Kierzkowski D et al. 2016. A mechanical feedback restricts sepal growth and shape in Arabidopsis.Curr. Biol 26:1019–28
    [Google Scholar]
  52. 52.  Himschoot E, Beeckman T, Friml J, Vanneste S 2015. Calcium is an organizer of cell polarity in plants. Biochim. Biophys. Acta 1853:2168–72
    [Google Scholar]
  53. 53.  Ho C-MK, Hotta T, Guo F, Roberson RW, Lee Y-RJ, Liu B 2011. Interaction of antiparallel microtubules in the phragmoplast is mediated by the microtubule-associated protein MAP65–3 in Arabidopsis. Plant Cell 23:2909–23
    [Google Scholar]
  54. 54.  Ho C-MK, Lee Y-RJ, Kiyama LD, Dinesh-Kumar SP, Liu B 2012. Arabidopsis microtubule-associated protein MAP65–3 cross-links antiparallel microtubules toward their plus ends in the phragmoplast via its distinct C-terminal microtubule binding domain. Plant Cell 24:2071–85
    [Google Scholar]
  55. 55.  Hong L, Dumond M, Zhu M, Tsugawa S, Li C-B et al. 2018. Heterogeneity and robustness in plant morphogenesis: from cells to organs. Annu. Rev. Plant Biol. 69:469–95
    [Google Scholar]
  56. 56.  Hong Z, Zhang Z, Olson JM, Verma DPS 2001. A novel UDP-glucose transferase is part of the callose synthase complex and interacts with phragmoplastin at the forming cell plate. Plant Cell 13:769–79
    [Google Scholar]
  57. 57.  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 222:157–65
    [Google Scholar]
  58. 58.  Hotta T, Kong Z, Ho C-MK, Zeng CJT, Horio T et al. 2012. Characterization of the Arabidopsis augmin complex uncovers its critical function in the assembly of the acentrosomal spindle and phragmoplast microtubule arrays. Plant Cell 24:1494–509
    [Google Scholar]
  59. 59.  Janski N, Masoud K, Batzenschlager M, Herzog E, Evrard JL et al. 2012. The GCP3-interacting proteins GIP1 and GIP2 are required for γ-tubulin complex protein localization, spindle integrity, and chromosomal stability. Plant Cell 24:1171–87
    [Google Scholar]
  60. 60.  Jürgens G 2005. Cytokinesis in higher plants. Annu. Rev. Plant Biol. 56:281–99
    [Google Scholar]
  61. 61.  Kaksonen M, Roux A 2018. Mechanisms of clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 19:313–26
    [Google Scholar]
  62. 62.  Karahara I, Staehelin LA, Mineyuki Y 2010. A role of endocytosis in plant cytokinesis. Commun. Integr. Biol. 3:36–38
    [Google Scholar]
  63. 63.  Karahara I, Suda J, Tahara H, Yokota E, Shimmen T et al. 2009. The preprophase band is a localized center of clathrin-mediated endocytosis in late prophase cells of the onion cotyledon epidermis. Plant J 57:819–31
    [Google Scholar]
  64. 64.  Karnahl M, Park M, Mayer U, Hiller U, Jürgens G 2017. ER assembly of SNARE complexes mediating formation of partitioning membrane in Arabidopsis cytokinesis. eLife 6:e25327Update on the mechanisms beyond sorting and targeting of SNARE complexes to the division plane and their functional implication in cell plate formation.
    [Google Scholar]
  65. 65.  Katsaros CI, Varvarigos V, Gachon CMM, Brand J, Motomura T et al. 2011. Comparative immunofluorescence and ultrastructural analysis of microtubule organization in Uronema sp., Klebsormidium flaccidum, K. subtilissimum, Stichococcus bacillaris and S. chloranthus (Chlorophyta). Protist 162:315–31
    [Google Scholar]
  66. 66.  Kawamura E, Himmelspach R, Rashbrooke MC, Whittington AT, Gale KR et al. 2006. MICROTUBULE ORGANIZATION 1 regulates structure and function of microtubule arrays during mitosis and cytokinesis in the Arabidopsis root. Plant Physiol 140:102–14
    [Google Scholar]
  67. 67.  Kirik V, Herrmann U, Parupalli C, Sedbrook JC, Ehrhardt DW, Hülskamp 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 120:4416–25
    [Google Scholar]
  68. 68.  Kohorn BD 2016. Cell wall-associated kinases and pectin perception. J. Exp. Bot. 67:489–94
    [Google Scholar]
  69. 69.  Kojo KH, Higaki T, Kutsuna N, Yoshida Y, Yasuhara H, Hasezawa S 2013. Roles of cortical actin microfilament patterning in division plane orientation in plants. Plant Cell Physiol 54:1491–503
    [Google Scholar]
  70. 70.  Komis G, Luptovčiak I, Ovečka M, Samakovli D, Šamajová O, Šamaj J 2017. Katanin effects on dynamics of cortical microtubules and mitotic arrays in Arabidopsis thaliana revealed by advanced live-cell imaging. Front. Plant Sci. 8:866
    [Google Scholar]
  71. 71.  Kosetsu K, de Keijzer J, Janson ME, Goshima G 2013. MICROTUBULE-ASSOCIATED PROTEIN65 is essential for maintenance of phragmoplast bipolarity and formation of the cell plate in Physcomitrella patens. Plant Cell 25:4479–92
    [Google Scholar]
  72. 72.  Kosetsu K, Murata T, Yamada M, Nishina M, Boruc J et al. 2017. Cytoplasmic MTOCs control spindle orientation for asymmetric cell division in plants. PNAS 114:E8847–54Cytoplasmic gametosomes, functioning analogously to polar prospindle caps, influence spindle and division plane orientation.
    [Google Scholar]
  73. 73.  Landrein B, Hamant O 2013. How mechanical stress controls microtubule behavior and morphogenesis in plants: history, experiments and revisited theories. Plant J 75:324–38
    [Google Scholar]
  74. 74.  Lau OS, Davies KA, Chang J, Adrian J, Rowe MH et al. 2014. Direct roles of SPEECHLESS in the specification of stomatal self-renewing cells. Science 345:1605–9
    [Google Scholar]
  75. 75.  Lau S, Slane D, Herud O, Kong J, Jürgens G 2012. Early embryogenesis in flowering plants: setting up the basic body pattern. Annu. Rev. Plant Biol. 63:483–506
    [Google Scholar]
  76. 76.  Lee YRJ, Giang HM, Liu B 2001. A novel plant kinesin-related protein specifically associates with the phragmoplast organelles. Plant Cell 13:2427–39
    [Google Scholar]
  77. 77.  Li H, Sun B, Sasabe M, Deng X, Machida Y et al. 2017. Arabidopsis MAP65–4 plays a role in phragmoplast microtubule organization and marks the cortical cell division site. New Phytol 215:187–201
    [Google Scholar]
  78. 78.  Li S, Sun T, Ren H 2015. The functions of the cytoskeleton and associated proteins during mitosis and cytokinesis in plant cells. Front. Plant Sci. 6:282
    [Google Scholar]
  79. 79.  Lin F, Krishnamoorthy P, Schubert V, Hause G, Heilmann M, Heilmann I 2019. A dual role for cell plate-associated PI4Kβ in endocytosis and phragmoplast dynamics during plant somatic cytokinesis. EMBO J 38:e100303Provides new insights into the coordination of cell plate assembly with phragmoplast dynamics.
    [Google Scholar]
  80. 80.  Lipka E, Gadeyne A, Stöckle D, Zimmermann S, De Jaeger G 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 26:2617–32
    [Google Scholar]
  81. 81.  Lloyd CW 1991. How does the cytoskeleton read the laws of geometry in aligning the division plane of plant cells?. Development 1:55–65
    [Google Scholar]
  82. 82.  Louveaux M, Hamant O 2013. The mechanics behind cell division. Curr. Opin. Plant Biol. 16:774–79
    [Google Scholar]
  83. 83.  Louveaux M, Julien JD, Mirabet V, Boudaoud A, Hamant O 2016. Cell division plane orientation based on tensile stress in Arabidopsis thaliana. PNAS 113:E4294–303Describes the impact of mechanical stress on preprophase band orientation and division planes.
    [Google Scholar]
  84. 84.  Lucas M, Kenobi K, von Wangenheim D, Voß U, Swarup K et al. 2013. Lateral root morphogenesis is dependent on the mechanical properties of the overlaying tissues. PNAS 110:5229–34
    [Google Scholar]
  85. 85.  Martinez P, Allsman LA, Brakke KA, Hoyt C, Hayes J et al. 2018. Predicting division planes of three-dimensional cells by soap-film minimization. Plant Cell 30:2255–66
    [Google Scholar]
  86. 86.  Martinez P, Luo A, Sylvester A, Rasmussen CG 2017. Proper division plane orientation and mitotic progression together allow normal growth of maize. PNAS 114:2759–64
    [Google Scholar]
  87. 87.  Mineyuki Y 1999. The preprophase band of microtubules: its function as a cytokinetic apparatus in higher plants. Int. Rev. Cytol. 187:1–49
    [Google Scholar]
  88. 88.  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. 97:527–37
    [Google Scholar]
  89. 89.  Mineyuki Y, Murata T, Wada M 1991. Experimental obliteration of the preprophase band alters the site of cell division, cell plate orientation, and phragmoplast expansion in Adiantum protonemata. J. Cell Sci. 100:551–57
    [Google Scholar]
  90. 90.  Mir R, Morris VH, Buschmann H, Rasmussen CG 2018. Division plane orientation defects revealed by a synthetic double mutant phenotype. Plant Physiol 176:418–31
    [Google Scholar]
  91. 91.  Molchan TM, Valster AH, Hepler PK 2002. Actomyosin promotes cell plate alignment and late lateral expansion in Tradescantia stamen hair cells. Planta 214:683–93
    [Google Scholar]
  92. 92.  Müller S 2012. Plant cell division. eLS 2012:a0023760
    [Google Scholar]
  93. 93.  Müller S 2012. Universal rules for division plane selection in plants. Protoplasma 249:239–53
    [Google Scholar]
  94. 94.  Müller S, Han S, Smith LG 2006. Two kinesins are involved in the spatial control of cytokinesis in Arabidopsis thaliana. Curr. Biol 16:888–94
    [Google Scholar]
  95. 95.  Müller S, Jürgens G 2016. Plant cytokinesis—no ring, no constriction but centrifugal construction of the partitioning membrane. Semin. Cell Dev. Biol. 53:10–18
    [Google Scholar]
  96. 96.  Müller S, Smertenko A, Wagner V, Heinrich M, Hussey PJ, Hauser MT 2004. The plant microtubule-associated protein AtMAP65–3/PLE is essential for cytokinetic phragmoplast function. Curr. Biol. 14:412–17
    [Google Scholar]
  97. 97.  Murata T, Sano T, Sasabe M, Nonaka S, Higashiyama T et al. 2013. Mechanism of microtubule array expansion in the cytokinetic phragmoplast. Nat. Commun. 4:1967
    [Google Scholar]
  98. 98.  Naito H, Goshima G 2015. NACK kinesin is required for metaphase chromosome alignment and cytokinesis in the moss Physcomitrella patens. Cell Struct. Funct 40:31–41
    [Google Scholar]
  99. 99.  Nakamura M, Yagi N, Kato T, Fujita S, Kawashima N et al. 2012. Arabidopsis GCP3-interacting protein 1/MOZART 1 is an integral component of the γ-tubulin-containing microtubule nucleating complex. Plant J 71:216–25
    [Google Scholar]
  100. 100.  Nishiyama T, Sakayama H, de Vries J, Buschmann H, Saint-Marcoux D et al. 2018. The Chara genome: secondary complexity and implications for plant terrestrialization. Cell 174:448–64.e24Evolutionary perspective on different cell division modes and explication of the presence of 221 genes implicated in preprophase and phragmoplast assembly and function.
    [Google Scholar]
  101. 101.  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. 24:419–24
    [Google Scholar]
  102. 102.  Ochs J, LaRue T, Tinaz B, Yongue C, Domozych DS 2014. The cortical cytoskeletal network and cell-wall dynamics in the unicellular charophycean green alga Penium margaritaceum. Ann. Bot 114:1237–49
    [Google Scholar]
  103. 103.  Otegui MS, Mastronarde DN, Kang B-H, Bednarek SY, Staehelin LA 2001. Three-dimensional analysis of syncytial-type cell plates during endosperm cellularization visualized by high resolution electron tomography. Plant Cell 13:2033–52
    [Google Scholar]
  104. 104.  Palevitz BA, Hepler PK 1974. The control of the plane of division during stomatal differentiation in Allium. Chromosoma 46:297–326
    [Google Scholar]
  105. 105.  Panteris E 2008. Cortical actin filaments at the division site of mitotic plant cells: a reconsideration of the ‘actin-depleted zone’. New Phytol 179:334–41
    [Google Scholar]
  106. 106.  Paredez AR, Somerville CR, Ehrhardt DW 2006. Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312:1491–95
    [Google Scholar]
  107. 107.  Park M, Touihri S, Müller I, Mayer U, Jürgens G 2012. Sec1/Munc18 protein stabilizes fusion-competent syntaxin for membrane fusion in Arabidopsis cytokinesis. Dev. Cell 22:989–1000
    [Google Scholar]
  108. 108.  Pickett-Heaps JD 1975. Green Algae: Structure, Reproduction, and Evolution in Selected Genera Sunderland, MA: Sinauer
    [Google Scholar]
  109. 109.  Pickett-Heaps JD, Gunning BES, Brown RC, Lemmon BE, Cleary AL 1999. The cytoplast concept in dividing plant cells: cytoplasmic domains and the evolution of spatially organized cell division. Am. J. Bot. 86:153–72
    [Google Scholar]
  110. 110.  Pickett-Heaps JD, Northcote DH 1966. Organization of microtubules and endoplasmic reticulum during mitosis and cytokinesis in wheat meristems. J. Cell Sci. 1:109–20
    [Google Scholar]
  111. 111.  Rasmussen CG, Bellinger M 2018. An overview of plant division-plane orientation. New Phytol 219:505–12
    [Google Scholar]
  112. 112.  Rasmussen CG, Humphries JA, Smith LG 2011. Determination of symmetric and asymmetric division planes in plant cells. Annu. Rev. Plant Biol. 62:387–409
    [Google Scholar]
  113. 113.  Rasmussen CG, Sun B, Smith LG 2011. Tangled localization at the cortical division site of plant cells occurs by several mechanisms. J. Cell Sci. 124:270–79
    [Google Scholar]
  114. 114.  Rasmussen CG, Wright AJ, Müller S 2013. The role of the cytoskeleton and associated proteins in plant cell division plane determination. Plant J 75:258–69
    [Google Scholar]
  115. 115.  Reichardt I, Stierhof YD, Mayer U, Richter S, Schwarz H et al. 2007. Plant cytokinesis requires de novo secretory trafficking but not endocytosis. Curr. Biol. 17:2047–53
    [Google Scholar]
  116. 116.  Reichelt S, Knight AE, Hodge TP, Baluska F, Samaj J et al. 1999. Characterization of the unconventional myosin VIII in plant cells and its localization at the post-cytokinetic cell wall. Plant J 19:555–67
    [Google Scholar]
  117. 117.  Richter S, Anders N, Wolters H, Beckmann H, Thomann A et al. 2010. Role of the GNOM gene in Arabidopsis apical-basal patterning—from mutant phenotype to cellular mechanism of protein action. Eur. J. Cell Biol. 89:138–44
    [Google Scholar]
  118. 118.  Richter S, Kientz M, Brumm S, Nielsen ME, Park M et al. 2014. Delivery of endocytosed proteins to the cell–division plane requires change of pathway from recycling to secretion. eLife 3:e02131
    [Google Scholar]
  119. 119.  Ruan Y, Wasteneys GO 2014. CLASP: a microtubule-based integrator of the hormone-mediated transitions from cell division to elongation. Curr. Opin. Plant Biol. 22:149–58
    [Google Scholar]
  120. 120.  Rybak K, Steiner A, Synek L, Klaeger S, Kulich I et al. 2014. Plant cytokinesis is orchestrated by the sequential action of the TRAPPII and exocyst tethering complexes. Dev. Cell 29:607–20
    [Google Scholar]
  121. 121.  Sampathkumar A, Krupinski P, Wightman R, Milani P, Berquand A et al. 2014. Subcellular and supracellular mechanical stress prescribes cytoskeleton behavior in Arabidopsis cotyledon pavement cells. eLife 3:e01967
    [Google Scholar]
  122. 122.  Samuels LA, Giddings TH, Staehelin AL 1995. Cytokinesis in tobacco BY-2 and root tip cells: a new model of cell plate formation in higher plants. J. Cell Biol. 130:1345–57
    [Google Scholar]
  123. 123.  Sasabe M, Kosetsu K, Hidaka M, Murase A, Machida Y 2011. Arabidopsis thaliana MAP65–1 and MAP65–2 function redundantly with MAP65–3/PLEIADE in cytokinesis downstream of MPK4. Plant Signal. Behav. 6:743–47
    [Google Scholar]
  124. 124.  Sasabe M, Machida Y 2012. Regulation of organization and function of microtubules by the mitogen-activated protein kinase cascade during plant cytokinesis. Cytoskeleton 69:913–18
    [Google Scholar]
  125. 125.  Sawitzky H, Grolig F 1995. Phragmoplast of the green alga Spirogyra is functionally distinct from the higher plant phragmoplast. J. Cell Biol. 130:1359–71
    [Google Scholar]
  126. 126.  Schaefer E, Belcram K, Uyttewaal M, Duroc Y, Goussot M et al. 2017. The preprophase band of microtubules controls the robustness of division orientation in plants. Science 356:186–89Characterizes a preprophase band–less mutant that displays neither defects in interphase cortical microtubule organization nor significant alterations in division plane orientations.
    [Google Scholar]
  127. 127.  Segui-Simarro JM, Austin JR II, White EA, Staehelin LA 2004. Electron tomographic analysis of somatic cell plate formation in meristematic cells of Arabidopsis preserved by high-pressure freezing. Plant Cell 16:836–56
    [Google Scholar]
  128. 128.  Sinnott EW, Bloch R 1940. Cytoplasmic behavior during division of vacuolate plant cells. PNAS 26:223–27
    [Google Scholar]
  129. 129.  Smertenko A, Assaad F, Baluška F, Bezanilla M, Buschmann H et al. 2017. Plant cytokinesis: terminology for structures and processes. Trends Cell Biol 27:885–94
    [Google Scholar]
  130. 130.  Smertenko A, Hewitt SL, Jacques CN, Kacprzyk R, Liu Y et al. 2018. Phragmoplast microtubule dynamics—a game of zones. J. Cell Sci. 131:jcs.203331
    [Google Scholar]
  131. 131.  Smertenko AP, Piette B, Hussey PJ 2011. The origin of phragmoplast asymmetry. Curr. Biol. 21:1924–30
    [Google Scholar]
  132. 132.  Spinner L, Gadeyne A, Belcram K, Goussot M, Moison M et al. 2013. A protein phosphatase 2A complex spatially controls plant cell division. Nat. Commun. 4:1863
    [Google Scholar]
  133. 133.  Spinner L, Pastuglia M, Belcram K, Pegoraro M, Goussot M et al. 2010. The function of TONNEAU1 in moss reveals ancient mechanisms of division plane specification and cell elongation in land plants. Development 137:2733–42
    [Google Scholar]
  134. 134.  Steiner A, Rybak K, Altmann M, McFarlane HE, Klaeger S et al. 2016. Cell cycle-regulated PLEIADE/AtMAP65–3 links membrane and microtubule dynamics during plant cytokinesis. Plant J 88:531–41
    [Google Scholar]
  135. 135.  Stöckle D, Herrmann A, Lipka E, Lauster T, Gavidia R et al. 2016. Putative RopGAPs impact division plane selection and interact with kinesin-12 POK1. Nat. Plants 2:16120
    [Google Scholar]
  136. 136.  Sun H, Furt F, Vidali L 2018. Myosin XI localizes at the mitotic spindle and along the cell plate during plant cell division in Physcomitrella patens. Biochem. Biophys. Res. Commun 506:409–21
    [Google Scholar]
  137. 137.  Takeuchi M, Karahara I, Kajimura N, Takaoka A, Murata K et al. 2016. Single microfilaments mediate the early steps of microtubule bundling during preprophase band formation in onion cotyledon epidermal cells. Mol. Biol. Cell 27:1809–20
    [Google Scholar]
  138. 138.  Tanaka H, Ishikawa M, Kitamura S, Takahashi Y, Soyano T et al. 2004. The AtNACK1/HINKEL and STUD/TETRASPORE/AtNACK2 genes, which encode functionally redundant kinesins, are essential for cytokinesis in Arabidopsis. Genes Cells 9:1199–211
    [Google Scholar]
  139. 139.  Timme RE, Bachvaroff TR, Delwiche CF 2012. Broad phylogenomic sampling and the sister lineage of land plants. PLOS ONE 7:e29696
    [Google Scholar]
  140. 140.  Torres-Ruiz RA, Jurgens G 1994. Mutations in the FASS gene uncouple pattern formation and morphogenesis in Arabidopsis development. Development 120:2967–78
    [Google Scholar]
  141. 141.  Traas J, Bellini C, Nacry P, Kronenberger J, Bouchez D, Caboche M 1995. Normal differentiation patterns in plants lacking microtubular preprophase bands. Nature 375:676–77
    [Google Scholar]
  142. 142.  Van Damme D, Coutuer S, De Rycke R, Bouget F-Y, Inzé D, Geelen D 2006. Somatic cytokinesis and pollen maturation in Arabidopsis depend on TPLATE, which has domains similar to coat proteins. Plant Cell 18:3502–18
    [Google Scholar]
  143. 143.  Van Damme D, Gadeyne A, Vanstraelen M, Inzé D, Van Montagu MCE et al. 2011. Adaptin-like protein TPLATE and clathrin recruitment during plant somatic cytokinesis occurs via two distinct pathways. PNAS 108:615–20
    [Google Scholar]
  144. 144.  Vermeer JEM, Geldner N 2015. Lateral root initiation in Arabidopsis thaliana: a force awakens. F1000Prime Rep 7:32
    [Google Scholar]
  145. 145.  von Dassow G 2009. Concurrent cues for cytokinetic furrow induction in animal cells. Trends Cell Biol 19:165–73
    [Google Scholar]
  146. 146.  Vos JW, Dogterom M, Emons AMC 2004. Microtubules become more dynamic but not shorter during preprophase band formation: a possible “search-and-capture” mechanism for microtubule translocation. Cytoskeleton 57:246–58
    [Google Scholar]
  147. 147.  Walker KL, Müller S, Moss D, Ehrhardt DW, Smith LG 2007. Arabidopsis TANGLED identifies the division plane throughout mitosis and cytokinesis. Curr. Biol. 17:1827–36
    [Google Scholar]
  148. 148.  Weingartner M, Pelayo HR, Binarova P, Zwerger K, Melikant B et al. 2003. A plant cyclin B2 is degraded early in mitosis and its ectopic expression shortens G2-phase and alleviates the DNA-damage checkpoint. J. Cell Sci. 116:487–98
    [Google Scholar]
  149. 149.  Whitewoods CD, Cammarata J, Nemec Venza Z, Sang S, Crook AD et al. 2018. CLAVATA was a genetic novelty for the morphological innovation of 3D growth in land plants. Curr. Biol. 28:2365–76.e5
    [Google Scholar]
  150. 150.  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 21:234–47
    [Google Scholar]
  151. 151.  Wu S-Z, Bezanilla M 2014. Myosin VIII associates with microtubule ends and together with actin plays a role in guiding plant cell division. eLife 3:e03498
    [Google Scholar]
  152. 152.  Xu XM, Zhao Q, Rodrigo-Peiris T, Brkljacic J, He CS et al. 2008. RanGAP1 is a continuous marker of the Arabidopsis cell division plane. PNAS 105:18637–42
    [Google Scholar]
  153. 153.  Yamada M, Tanaka-Takiguchi Y, Hayashi M, Nishina M, Goshima G 2017. Multiple kinesin-14 family members drive microtubule minus end–directed transport in plant cells. J. Cell Biol. 216:1705–14
    [Google Scholar]
  154. 154.  Yoneda A, Akatsuka M, Hoshino H, Kumagai F, Hasezawa S 2005. Decision of spindle poles and division plane by double preprophase bands in a BY-2 cell line expressing GFP–tubulin. Plant Cell Physiol 46:531–38
    [Google Scholar]
  155. 155.  Yoshida S, Barbier de Reuille P, Lane B, Bassel GW, Prusinkiewicz P et al. 2014. Genetic control of plant development by overriding a geometric division rule. Dev. Cell 29:75–87
    [Google Scholar]
  156. 156.  Zhang H, Deng X, Sun B, Lee Van S, Kang Z et al. 2018. Role of the BUB3 protein in phragmoplast microtubule reorganization during cytokinesis. Nat. Plants 4:485–94Reports an unexpected function of Arabidopsis BUB3.1 and BUB3.2 in the regulation of MAP65–3 phragmoplast localization.
    [Google Scholar]
  157. 157.  Zhao F, Chen W, Traas J 2018. Mechanical signaling in plant morphogenesis. Curr. Opin. Genet. Dev. 51:26–30
    [Google Scholar]
/content/journals/10.1146/annurev-arplant-050718-100444
Loading
/content/journals/10.1146/annurev-arplant-050718-100444
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error