1932

Abstract

In contrast to well-studied fungal and animal cells, plant cells assemble bipolar spindles that exhibit a great deal of plasticity in the absence of structurally defined microtubule-organizing centers like the centrosome. While plants employ some evolutionarily conserved proteins to regulate spindle morphogenesis and remodeling, many essential spindle assembly factors found in vertebrates are either missing or not required for producing the plant bipolar microtubule array. Plants also produce proteins distantly related to their fungal and animal counterparts to regulate critical events such as the spindle assembly checkpoint. Plant spindle assembly initiates with microtubule nucleation on the nuclear envelope followed by bipolarization into the prophase spindle. After nuclear envelope breakdown, kinetochore fibers are assembled and unified into the spindle apparatus with convergent poles. Of note, compared to fungal and animal systems, relatively little is known about how plant cells remodel the spindle microtubule array during anaphase. Uncovering mitotic functions of novel proteins for spindle assembly in plants will illuminate both common and divergent mechanisms employed by different eukaryotic organisms to segregate genetic materials.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-070721-084258
2022-05-20
2024-06-16
Loading full text...

Full text loading...

/deliver/fulltext/arplant/73/1/annurev-arplant-070721-084258.html?itemId=/content/journals/10.1146/annurev-arplant-070721-084258&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Alfaro-Aco R, Thawani A, Petry S. 2017. Structural analysis of the role of TPX2 in branching microtubule nucleation. J. Cell Biol. 216:983–97
    [Google Scholar]
  2. 2.
    Ambrose JC, Cyr R. 2007. The kinesin ATK5 functions in early spindle assembly in Arabidopsis. Plant Cell 19:226–36
    [Google Scholar]
  3. 3.
    Ambrose JC, Cyr R. 2008. Mitotic spindle organization by the preprophase band. Mol. Plant 1:950–60
    [Google Scholar]
  4. 4.
    Ambrose JC, Li W, Marcus A, Ma H, Cyr R 2005. A minus-end-directed kinesin with plus-end tracking protein activity is involved in spindle morphogenesis. Mol. Biol. Cell 16:1584–92
    [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 19:2763–75
    [Google Scholar]
  6. 6.
    Apostolakos P, Galatis B 1985. Studies on the development of the air pores and air chambers of Marchantia paleacea. III. Microtubule organization in preprophase-prophase initial aperture cells—formation of incomplete preprophase microtubule bands. Protoplasma 128:120–35
    [Google Scholar]
  7. 7.
    Asada T, Kuriyama R, Shibaoka H. 1997. TKRP125, a kinesin-related protein involved in the centrosome-independent organization of the cytokinetic apparatus in tobacco BY-2 cells. J. Cell Sci. 110:179–89
    [Google Scholar]
  8. 8.
    Ashtiyani RK, Moghaddam AMB, Schubert V, Rutten T, Fuchs J et al. 2011. AtHaspin phosphorylates histone H3 at threonine 3 during mitosis and contributes to embryonic patterning in Arabidopsis. Plant J. 68:443–54
    [Google Scholar]
  9. 9.
    Bajer A. 1968. Behavior and fine structure of spindle fibers during mitosis in endosperm. Chromosoma 25:249–81
    [Google Scholar]
  10. 10.
    Bajer A. 1990. The elusive organization of the spindle and kinetochore fiber: a conceptual retrospect. Adv. Cell Biol. 3:65–93Summarizes the kinetochore fiber as an autonomous fir tree–like complex with skewed microtubules growing out of those fibers attached to the kinetochore.
    [Google Scholar]
  11. 11.
    Bajer AS, Mole-Bajer J. 1989. Microtubules modify kinetochore fiber organization and function: a new aspect of mitosis. Prog. Clin. Biol. Res. 318:171–84
    [Google Scholar]
  12. 12.
    Bannigan A, Lizotte-Waniewski M, Riley M, Baskin TI 2008. Emerging molecular mechanisms that power and regulate the anastral mitotic spindle of flowering plants. Cell Motil. Cytoskelet. 65:1–11
    [Google Scholar]
  13. 13.
    Bannigan A, Scheible W-R, Lukowitz W, Fagerstrom C, Wadsworth P et al. 2007. A conserved role for kinesin-5 in plant mitosis. J. Cell Sci. 120:2819–27
    [Google Scholar]
  14. 14.
    Barroso C, Chan J, Allan V, Doonan J, Hussey P, Lloyd C. 2000. Two kinesin-related proteins associated with the cold-stable cytoskeleton of carrot cells: characterization of a novel kinesin, DcKRP120-2. Plant J. 24:859–68
    [Google Scholar]
  15. 15.
    Baskin TI, Cande WZ. 1990. The structure and function of the mitotic spindle in flowering plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 41:277–315
    [Google Scholar]
  16. 16.
    Bisgrove SR, Lee Y-RJ, 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
    [Google Scholar]
  17. 17.
    Boleti H, Karsenti E, Vernos I 1996. Xklp2, a novel Xenopus centrosomal kinesin-like protein required for centrosome separation during mitosis. Cell 84:49–59
    [Google Scholar]
  18. 18.
    Boruc J, Deng X, Mylle E, Besbrugge N, Van Durme M et al. 2019. TPX2-LIKE PROTEIN 3 is the primary activator of α-Aurora kinases and is essential for embryogenesis. Plant Physiol. 180:1389–405The evolutionarily conserved TPX2 does not play a critical role in plant mitosis; the related but divergent TPXL3 protein activates Aurora kinase's function in spindles.
    [Google Scholar]
  19. 19.
    Boruc J, Mylle E, Duda M, De Clercq R, Rombauts S et al. 2010. Systematic localization of the Arabidopsis core cell cycle proteins reveals novel cell division complexes. Plant Physiol. 152:553–65
    [Google Scholar]
  20. 20.
    Brenner S, Pepper D, Berns MW, Tan E, Brinkley BR 1981. Kinetochore structure, duplication, and distribution in mammalian cells: analysis by human autoantibodies from scleroderma patients. J. Cell Biol. 91:95–102
    [Google Scholar]
  21. 21.
    Brown RC, Lemmon BE. 1989. Minispindles and cytoplasmic domains in microsporogenesis of orchids. Protoplasma 148:26–32
    [Google Scholar]
  22. 22.
    Brown RC, Lemmon BE. 2007. The pleiomorphic plant MTOC: an evolutionary perspective. J. Integr. Plant Biol. 49:1142–53
    [Google Scholar]
  23. 23.
    Bulankova P, Akimcheva S, Fellner N, Riha K. 2013. Identification of Arabidopsis meiotic cyclins reveals functional diversification among plant cyclin genes. PLOS Genet. 9:e1003508
    [Google Scholar]
  24. 24.
    Burk DH, Liu B, Zhong R, Morrison WH, Ye ZH. 2001. A katanin-like protein regulates normal cell wall biosynthesis and cell elongation. Plant Cell 13:807–27Concludes that plants employ proteins other than the conserved microtubule-severing enzyme katanin to induce rapid microtubule turnovers.
    [Google Scholar]
  25. 25.
    Buschmann H, Fabri CO, Hauptmann M, Hutzler P, Laux T et al. 2004. Helical growth of the Arabidopsis mutant tortifolia1 reveals a plant-specific microtubule-associated protein. Curr. Biol. 14:1515–21
    [Google Scholar]
  26. 26.
    Carmena M, Wheelock M, Funabiki H, Earnshaw WC. 2012. The chromosomal passenger complex (CPC): from easy rider to the godfather of mitosis. Nat. Rev. Mol. Cell Biol. 13:789–803
    [Google Scholar]
  27. 27.
    Cavazza T, Vernos I. 2015. The RanGTP pathway: from nucleo-cytoplasmic transport to spindle assembly and beyond. Front. Cell Dev. Biol. 3:82
    [Google Scholar]
  28. 28.
    Chen CB, Marcus A, Li WX, Hu Y, Calzada J-PV et al. 2002. The Arabidopsis ATK1 gene is required for spindle morphogenesis in male meiosis. Development 129:2401–9
    [Google Scholar]
  29. 29.
    Cleveland DW, Mao Y, Sullivan KF 2003. Centromeres and kinetochores: from epigenetics to mitotic checkpoint signaling. Cell 112:407–21
    [Google Scholar]
  30. 30.
    Currie CE, Mora-Santos M, Smith CA, McAinsh AD, Millar JBA. 2018. Bub1 is not essential for the checkpoint response to unattached kinetochores in diploid human cells. Curr. Biol. 28:R909–30
    [Google Scholar]
  31. 31.
    Dawe RK, Reed LM, Yu HG, Muszynski MG, Hiatt EN. 1999. A maize homolog of mammalian CENPC is a constitutive component of the inner kinetochore. Plant Cell 11:1227–38
    [Google Scholar]
  32. 32.
    Demidov D, Van Damme D, Geelen D, Blattner FR, Houben A. 2005. Identification and dynamics of two classes of Aurora-like kinases in Arabidopsis and other plants. Plant Cell 17:836–48
    [Google Scholar]
  33. 33.
    Deng X, Higaki T, Lin H-H, Lee Y-RJ, Liu B. 2021. Acentrosomal spindle morphogenesis is dependent on the unconventional TPX2 family protein TPXL3 and α Aurora kinase in Arabidopsis thaliana. Res. Sq. https://doi.org/10.21203/rs.3.rs-519922/v1
    [Crossref] [Google Scholar]
  34. 34.
    Enos AP, Morris NR. 1990. Mutation of a gene that encodes a kinesin-like protein blocks nuclear division in A. nidulans. Cell 60:1019–27
    [Google Scholar]
  35. 35.
    Fowke LC, Pickett-Heaps JD. 1978. Electron microscope study of vegetative cell division in two species of Marchantia. Can. J. Bot. 56:467–75
    [Google Scholar]
  36. 36.
    Gard DL, Becker BE, Romney SJ. 2004. MAPping the eukaryotic tree of life: structure, function, and evolution of the MAP215/Dis1 family of microtubule-associated proteins. Int. Rev. Cytol. 239:179–272
    [Google Scholar]
  37. 37.
    Gillmor CS, Roeder AH, Sieber P, Somerville C, Lukowitz W. 2016. A genetic screen for mutations affecting cell division in the Arabidopsis thaliana embryo identifies seven loci required for cytokinesis. PLOS ONE 11:e0146492
    [Google Scholar]
  38. 38.
    Goshima G, Mayer M, Zhang N, Stuurman N, Vale RD 2008. Augmin: a protein complex required for centrosome-independent microtubule generation within the spindle. J. Cell Biol. 181:421–29
    [Google Scholar]
  39. 39.
    Guo L, Ho CM, Kong Z, Lee Y-RJ, Qian Q, Liu B 2009. Evaluating the microtubule cytoskeleton and its interacting proteins in monocots by mining the rice genome. Ann. Bot. 103:387–402
    [Google Scholar]
  40. 40.
    Hamada T, Igarashi H, Itoh TJ, Shimmen T, Sonobe S. 2004. Characterization of a 200 kDa microtubule-associated protein of tobacco BY-2 cells, a member of the XMAP215/MOR1 family. Plant Cell Physiol. 45:1233–42
    [Google Scholar]
  41. 41.
    Hamada T, Nagasaki-Takeuchi N, Kato T, Fujiwara M, Sonobe S et al. 2013. Purification and characterization of novel microtubule-associated proteins from Arabidopsis cell suspension cultures. Plant Physiol. 163:1804–16
    [Google Scholar]
  42. 42.
    Hara M, Fukagawa T. 2020. Dynamics of kinetochore structure and its regulations during mitotic progression. Cell. Mol. Life Sci. 77:2981–95
    [Google Scholar]
  43. 43.
    Hayashi T, Sano T, Kutsuna N, Kumagai-Sano F, Hasezawa S. 2007. Contribution of anaphase B to chromosome separation in higher plant cells estimated by image processing. Plant Cell Physiol. 48:1509–13
    [Google Scholar]
  44. 44.
    Helgeson LA, Zelter A, Riffle M, MacCoss MJ, Asbury CL, Davis TN. 2018. Human Ska complex and Ndc80 complex interact to form a load-bearing assembly that strengthens kinetochore–microtubule attachments. PNAS 115:2740–45
    [Google Scholar]
  45. 45.
    Herrmann A, Livanos P, Zimmermann S, Berendzen K, Rohr L et al. 2021. KINESIN-12E regulates metaphase spindle flux and helps control spindle size in Arabidopsis. Plant Cell 33:27–43
    [Google Scholar]
  46. 46.
    Higgins DM, Nannas NJ, Dawe RK. 2016. The maize Divergent spindle-1 (dv1) gene encodes a kinesin-14A motor protein required for meiotic spindle pole organization. Front. Plant Sci. 7:1277
    [Google Scholar]
  47. 47.
    Ho CMK, 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]
  48. 48.
    Ho CMK, Hotta T, Kong Z, Zeng CJ, Sun J et al. 2011. Augmin plays a critical role in organizing the spindle and phragmoplast microtubule arrays in Arabidopsis. Plant Cell 23:2606–18
    [Google Scholar]
  49. 49.
    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 24:1494–509Functional characterization of the plant augmin complex concludes that there is an evolutionarily conserved mechanism of microtubule-dependent microtubule generation in plant spindle assembly.
    [Google Scholar]
  50. 50.
    Huang Y, Wang H, Huang X, Wang Q, Wang J et al. 2019. Maize VKS1 regulates mitosis and cytokinesis during early endosperm development. Plant Cell 31:1238–56
    [Google Scholar]
  51. 51.
    Inoue S. 1981. Cell division and the mitotic spindle. J. Cell Biol. 91:131s–47s
    [Google Scholar]
  52. 52.
    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]
  53. 53.
    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]
  54. 54.
    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]
  55. 55.
    Kirioukhova O, Johnston AJ, Kleen D, Kagi C, Baskar R et al. 2011. Female gametophytic cell specification and seed development require the function of the putative Arabidopsis INCENP ortholog WYRD. Development 138:3409–20
    [Google Scholar]
  56. 56.
    Komaki S, Abe T, Coutuer S, Inzé D, Russinova E, Hashimoto T 2010. Nuclear-localized subtype of end-binding 1 protein regulates spindle organization in Arabidopsis. J. Cell Sci. 123:451–59
    [Google Scholar]
  57. 57.
    Komaki S, Schnittger A. 2017. The spindle assembly checkpoint in Arabidopsis is rapidly shut off during severe stress. Dev. Cell 43:172–85.E5Dissection of proteins associated with the spindle assembly checkpoint (SAC) in plant mitosis leads to the discovery of novel aspects of SAC regulation.
    [Google Scholar]
  58. 58.
    Komaki S, Takeuchi H, Hamamura Y, Heese M, Hashimoto T, Schnittger A. 2020. Functional analysis of the plant chromosomal passenger complex. Plant Physiol. 183:1586–99
    [Google Scholar]
  59. 59.
    Kong Z, Hotta T, Lee Y-RJ, Horio T, Liu B 2010. The γ-tubulin complex protein GCP4 is required for organizing functional microtubule arrays in Arabidopsis thaliana. Plant Cell 22:191–204
    [Google Scholar]
  60. 60.
    Kong Z, Ioki M, Braybrook S, Li S, Ye ZH et al. 2015. Kinesin-4 functions in vesicular transport on cortical microtubules and regulates cell wall mechanics during cell elongation in plants. Mol. Plant 8:1011–23Concludes that Kinesin-4 is dispensable in plant mitosis.
    [Google Scholar]
  61. 61.
    Kops GJPL, Gassmann R. 2020. Crowning the kinetochore: the fibrous corona in chromosome segregation. Trends Cell Biol. 30:653–67
    [Google Scholar]
  62. 62.
    Kops GJPL, Snel B, Tromer EC. 2020. Evolutionary dynamics of the spindle assembly checkpoint in eukaryotes. Curr. Biol. 30:R589–602
    [Google Scholar]
  63. 63.
    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:E8847–54
    [Google Scholar]
  64. 64.
    Kozgunova E, Nishina M, Goshima G. 2019. Kinetochore protein depletion underlies cytokinesis failure and somatic polyploidization in the moss Physcomitrella patens. eLife 8:e43652
    [Google Scholar]
  65. 65.
    Krupnova T, Sasabe M, Ghebreghiorghis L, Gruber CW, Hamada T et al. 2009. Microtubule-associated kinase-like protein RUNKEL needed for cell plate expansion in Arabidopsis cytokinesis. Curr. Biol. 19:518–23
    [Google Scholar]
  66. 66.
    Kurihara D, Matsunaga S, Omura T, Higashiyama T, Fukui K. 2011. Identification and characterization of plant Haspin kinase as a histone H3 threonine kinase. BMC Plant Biol. 11:73
    [Google Scholar]
  67. 67.
    Lawrence EJ, Zanic M, Rice LM 2020. CLASPs at a glance. J. Cell Sci. 133:jcs243097
    [Google Scholar]
  68. 68.
    Lecland N, Lüders J. 2014. The dynamics of microtubule minus ends in the human mitotic spindle. Nat. Cell Biol. 16:770–78
    [Google Scholar]
  69. 69.
    Lee Y-RJ, Hiwatashi Y, Hotta T, Xie T, Doonan JH, Liu B. 2017. The mitotic function of augmin is dependent on its microtubule-associated protein subunit EDE1 in Arabidopsis thaliana. Curr. Biol. 27:3891–97.E4
    [Google Scholar]
  70. 70.
    Lee Y-RJ, Li Y, Liu B 2007. Two Arabidopsis phragmoplast-associated kinesins play a critical role in cytokinesis during male gametogenesis. Plant Cell 19:2595–605
    [Google Scholar]
  71. 71.
    Lee Y-RJ, Liu B. 2013. The rise and fall of the phragmoplast microtubule array. Curr. Opin. Plant Biol. 16:757–63
    [Google Scholar]
  72. 72.
    Lee Y-RJ, Liu B. 2019. Microtubule nucleation for the assembly of acentrosomal microtubule arrays in plant cells. New Phytol. 222:1705–18
    [Google Scholar]
  73. 73.
    Lee Y-RJ, Qiu W, Liu B 2015. Kinesin motors in plants: from subcellular dynamics to motility regulation. Curr. Opin. Plant Biol. 28:120–26
    [Google Scholar]
  74. 74.
    Leong SY, Edzuka T, Goshima G, Yamada M 2020. Kinesin-13 and Kinesin-8 function during cell growth and division in the moss Physcomitrella patens. Plant Cell 32:683–702Provides evidence demonstrating that neither Kinesin-8 nor Kinesin-13 is an important regulator of spindle assembly in moss cells.
    [Google Scholar]
  75. 75.
    Lermontova I, Fuchs J, Schubert I. 2008. The Arabidopsis checkpoint protein Bub3.1 is essential for gametophyte development. Front. Biosci. 13:5202–11
    [Google Scholar]
  76. 76.
    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]
  77. 77.
    Li L, Shimada T, Takahashi H, Koumoto Y, Shirakawa M et al. 2013. MAG2 and three MAG2-INTERACTING PROTEINs form an ER-localized complex to facilitate storage protein transport in Arabidopsis thaliana. Plant J. 76:781–91
    [Google Scholar]
  78. 78.
    Liu B, Palevitz BA. 1991. Kinetochore fiber formation in dividing generative cells of Tradescantia kinetochore reorientation associated with the transition between lateral microtubule interactions and end-on kinetochore fibers. J. Cell Sci. 98:475–82
    [Google Scholar]
  79. 79.
    Liu B, Palevitz BA. 1992. Organization of cortical microfilaments in dividing root cells. Cell Motil. Cytoskelet. 23:252–64
    [Google Scholar]
  80. 80.
    Liu P, Würtz M, Zupa E, Pfeffer S, Schiebel E. 2021. Microtubule nucleation: the waltz between γ-tubulin ring complex and associated proteins. Curr. Opin. Cell Biol. 68:124–31
    [Google Scholar]
  81. 81.
    Liu T, Tian J, Wang G, Yu Y, Wang C et al. 2014. Augmin triggers microtubule-dependent microtubule nucleation in interphase plant cells. Curr. Biol. 24:2708–13
    [Google Scholar]
  82. 82.
    Lloyd CW. 1987. The plant cytoskeleton: the impact of fluorescence microscopy. Annu. Rev. Plant Physiol. 38:119–39
    [Google Scholar]
  83. 83.
    London N, Biggins S. 2014. Signalling dynamics in the spindle checkpoint response. Nat. Rev. Mol. Cell Biol. 15:736–47
    [Google Scholar]
  84. 84.
    Lu L, Lee Y-RJ, Pan R, Maloof JN, Liu B. 2005. An internal motor kinesin is associated with the Golgi apparatus and plays a role in trichome morphogenesis in Arabidopsis. Mol. Biol. Cell 16:811–23
    [Google Scholar]
  85. 85.
    Luo Y, Ahmad E, Liu ST 2018. MAD1: kinetochore receptors and catalytic mechanisms. Front. Cell Dev. Biol. 6:51
    [Google Scholar]
  86. 86.
    Marcus A, Li W, Ma H, Cyr RJ 2003. A kinesin mutant with an atypical bipolar spindle undergoes normal mitosis. Mol. Biol. Cell 14:1717–26
    [Google Scholar]
  87. 87.
    Martinez P, Dixit R, Balkunde RS, Zhang A, O'Leary SE et al. 2020. TANGLED1 mediates microtubule interactions that may promote division plane positioning in maize. J. Cell Biol. 219:e201907184
    [Google Scholar]
  88. 88.
    Mazia D. 1984. Centrosomes and mitotic poles. Exp. Cell Res. 153:1–15
    [Google Scholar]
  89. 89.
    McIntosh JR. 2021. Anaphase A. Semin. Cell Dev. Biol. 117:118–26
    [Google Scholar]
  90. 90.
    McNally FJ, Roll-Mecak A. 2018. Microtubule-severing enzymes: from cellular functions to molecular mechanism. J. Cell Biol. 217:4057–69
    [Google Scholar]
  91. 91.
    Miao HY, Guo RF, Chen JL, Wang QM, Lee Y-RJ, Liu B. 2019. The γ-tubulin complex protein GCP6 is crucial for spindle morphogenesis but not essential for microtubule reorganization in Arabidopsis. PNAS 116:27115–23Shows that the γ-tubulin ring complex (γ-TuRC) and other novel forms of the γ-tubulin complex function in microtubule nucleation inside the spindle apparatus.
    [Google Scholar]
  92. 92.
    Miki T, Naito H, Nishina M, Goshima G. 2014. Endogenous localizome identifies 43 mitotic kinesins in a plant cell. PNAS 111:E1053–61
    [Google Scholar]
  93. 93.
    Mishra RK, Chakraborty P, Arnaoutov A, Fontoura BMA, Dasso M. 2010. The Nup107-160 complex and γ-TuRC regulate microtubule polymerization at kinetochores. Nat. Cell Biol. 12:164–69
    [Google Scholar]
  94. 94.
    Molé-Bajer J, Bajer AS, Inoué S. 1988. Three-dimensional localization and redistribution of F-actin in higher plant mitosis and cell plate formation. Cell Motil. Cytoskelet. 10:217–28
    [Google Scholar]
  95. 95.
    Mole-Bajer J, Bajer AS, Zinkowski RP, Balczon RD, Brinkley BR. 1990. Autoantibodies from a patient with scleroderma CREST recognized kinetochores of the higher plant Haemanthus. PNAS 87:3599–603
    [Google Scholar]
  96. 96.
    Moschou PN, Gutierrez-Beltran E, Bozhkov PV, Smertenko A. 2016. Separase promotes microtubule polymerization by activating CENP-E-related kinesin Kin7. Dev. Cell 37:350–61
    [Google Scholar]
  97. 97.
    Motose H, Hamada T, Yoshimoto K, Murata T, Hasebe M et al. 2011. NIMA-related kinases 6, 4, and 5 interact with each other to regulate microtubule organization during epidermal cell expansion in Arabidopsis thaliana. Plant J. 67:993–1005
    [Google Scholar]
  98. 98.
    Müller S, Livanos P. 2019. Plant kinesin-12: localization heterogeneity and functional implications. Int. J. Mol. Sci. 20:4213
    [Google Scholar]
  99. 99.
    Murata T, Sonobe S, Baskin TI, Hyodo S, Hasezawa S et al. 2005. Microtubule-dependent microtubule nucleation based on recruitment of γ-tubulin in higher plants. Nat. Cell Biol. 7:961–68
    [Google Scholar]
  100. 100.
    Musacchio A. 2015. The molecular biology of spindle assembly checkpoint signaling dynamics. Curr. Biol. 25:R1002–18
    [Google Scholar]
  101. 101.
    Nakajima K, Furutani I, Tachimoto H, Matsubara H, Hashimoto T. 2004. SPIRAL1 encodes a plant-specific microtubule-localized protein required for directional control of rapidly expanding Arabidopsis cells. Plant Cell 16:1178–90
    [Google Scholar]
  102. 102.
    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]
  103. 103.
    Nakaoka Y, Miki T, Fujioka R, Uehara R, Tomioka A et al. 2012. An inducible RNA interference system in Physcomitrella patens reveals a dominant role of augmin in phragmoplast microtubule generation. Plant Cell 24:1478–93
    [Google Scholar]
  104. 104.
    Nebenfuhr A, Dixit R. 2018. Kinesins and myosins: molecular motors that coordinate cellular functions in plants. Annu. Rev. Plant Biol. 69:329–61
    [Google Scholar]
  105. 105.
    Oakley BR, Paolillo V, Zheng Y 2015. γ-Tubulin complexes in microtubule nucleation and beyond. Mol. Biol. Cell 26:2957–62
    [Google Scholar]
  106. 106.
    Oda Y, Fukuda H 2013. Rho of plant GTPase signaling regulates the behavior of Arabidopsis Kinesin-13A to establish secondary cell wall patterns. Plant Cell 25:4439–50
    [Google Scholar]
  107. 107.
    Oh SA, Pal MD, Park SK, Johnson JA, Twell D 2010. The tobacco MAP215/Dis1-family protein TMBP200 is required for the functional organization of microtubule arrays during male germline establishment. J. Exp. Bot. 61:969–81
    [Google Scholar]
  108. 108.
    Palevitz BA. 1990. Kinetochore behavior during generative cell division in Tradescantia virginiana. Protoplasma 157:120–27
    [Google Scholar]
  109. 109.
    Palevitz BA. 1993. Morphological plasticity of the mitotic apparatus in plants and its developmental consequences. Plant Cell 5:1001–9
    [Google Scholar]
  110. 110.
    Panteris E, Adamakis I-DS. 2012. Aberrant microtubule organization in dividing root cells of p60-katanin mutants. Plant Signal Behav. 7:16–18
    [Google Scholar]
  111. 111.
    Park GT, Frost JM, Park J-S, Kim TH, Lee JS et al. 2014. Nucleoporin MOS7/Nup88 is required for mitosis in gametogenesis and seed development in Arabidopsis. PNAS 111:18393–98
    [Google Scholar]
  112. 112.
    Pastuglia M, Azimzadeh J, Goussot M, Camilleri C, Belcram K et al. 2006. γ-Tubulin is essential for microtubule organization and development in Arabidopsis. Plant Cell 18:1412–25
    [Google Scholar]
  113. 113.
    Petrovská B, Jeřábková H, Kohoutová L, Cenklová V, Pochylová Z et al. 2013. Overexpressed TPX2 causes ectopic formation of microtubular arrays in the nuclei of acentrosomal plant cells. J. Exp. Bot. 64:4575–87
    [Google Scholar]
  114. 114.
    Pickett-Heaps J, Forer A. 2009. Mitosis: spindle evolution and the matrix model. Protoplasma 235:91–99
    [Google Scholar]
  115. 115.
    Pickett-Heaps JD. 1969. The evolution of the mitotic apparatus: an attempt at comparative ultrastructural cytology in dividing plant cells. Cytobios 3:257–80
    [Google Scholar]
  116. 116.
    Polak B, Risteski P, Lesjak S, Tolić IM 2017. PRC1-labeled microtubule bundles and kinetochore pairs show one-to-one association in metaphase. EMBO Rep. 18:217–30
    [Google Scholar]
  117. 117.
    Quan L, Xiao R, Li W, Oh S-A, Kong H et al. 2008. Functional divergence of the duplicated AtKIN14a and AtKIN14b genes: critical roles in Arabidopsis meiosis and gametophyte development. Plant J. 53:1013–26
    [Google Scholar]
  118. 118.
    Raaijmakers JA, Medema RH. 2014. Function and regulation of dynein in mitotic chromosome segregation. Chromosoma 123:407–22
    [Google Scholar]
  119. 119.
    Richardson DN, Simmons MP, Reddy ASN. 2006. Comprehensive comparative analysis of kinesins in photosynthetic eukaryotes. BMC Genom. 7:18
    [Google Scholar]
  120. 120.
    Rogers SL, Rogers GC, Sharp DJ, Vale RD. 2002. Drosophila EB1 is important for proper assembly, dynamics, and positioning of the mitotic spindle. J. Cell Biol. 158:873–84
    [Google Scholar]
  121. 121.
    Sasaki T, Tsutsumi M, Otomo K, Murata T, Yagi N et al. 2019. A novel katanin-tethering machinery accelerates cytokinesis. Curr. Biol. 29:4060–70.e3
    [Google Scholar]
  122. 122.
    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 356:186–89
    [Google Scholar]
  123. 123.
    Scholey JM, Civelekoglu-Scholey G, Brust-Mascher I. 2016. Anaphase B. Biology 5:51
    [Google Scholar]
  124. 124.
    She ZY, Yang WX. 2017. Molecular mechanisms of kinesin-14 motors in spindle assembly and chromosome segregation. J. Cell Sci. 130:2097–110
    [Google Scholar]
  125. 125.
    Shoji T, Narita NN, Hayashi K, Asada J, Hamada T et al. 2004. Plant-specific microtubule-associated protein SPIRAL2 is required for anisotropic growth in Arabidopsis. Plant Physiol. 136:3933–44
    [Google Scholar]
  126. 126.
    Simunić J, Tolić IM. 2016. Mitotic spindle assembly: building the bridge between sister K-fibers. Trends Biochem. Sci. 41:824–33
    [Google Scholar]
  127. 127.
    Smertenko AP, Chang H-Y, Sonobe S, Fenyk SI, Weingartner M et al. 2006. Control of the AtMAP65-1 interaction with microtubules through the cell cycle. J. Cell Sci. 119:3227–37
    [Google Scholar]
  128. 128.
    Smertenko AP, Kaloriti D, Chang H-Y, Fiserova J, Opatrny Z, Hussey PJ 2008. The C-terminal variable region specifies the dynamic properties of Arabidopsis microtubule-associated protein MAP65 isotypes. Plant Cell 20:3346–58
    [Google Scholar]
  129. 129.
    Smirnova EA, Bajer AS. 1992. Spindle poles in higher plant mitosis. Cell Motil. Cytoskelet. 23:1–7
    [Google Scholar]
  130. 130.
    Smirnova EA, Bajer AS. 1994. Microtubule converging centers and reorganization of the interphase cytoskeleton and the mitotic spindle in higher plant Haemanthus. Cell Motil. Cytoskelet. 27:219–33
    [Google Scholar]
  131. 131.
    Smirnova EA, Bajer AS. 1998. Early stages of spindle formation and independence of chromosome and microtubule cycles in Haemanthus endosperm. Cell Motil. Cytoskelet. 40:22–37
    [Google Scholar]
  132. 132.
    So C, Seres KB, Steyer AM, Mönnich E, Clift D et al. 2019. A liquid-like spindle domain promotes acentrosomal spindle assembly in mammalian oocytes. Science 364eaat9557Microtubule-linked factors of microtubule-associated proteins (MAPs), motors, and regulatory proteins form a liquid-like spindle domain that serves as an acentriolar microtubule-organizing center in female meiosis in frogs.
    [Google Scholar]
  133. 133.
    Starr DA, Williams BC, Li Z, Etemad-Moghadam B, Dawe RK, Goldberg ML. 1997. Conservation of the centromere/kinetochore protein ZW10. J. Cell Biol. 138:1289–301
    [Google Scholar]
  134. 134.
    Su H, Liu Y, Wang C, Liu Y, Feng C et al. 2021. Knl1 participates in spindle assembly checkpoint signaling in maize. PNAS 118:e2022357118
    [Google Scholar]
  135. 135.
    Sweeney HL, Holzbaur ELF. 2018. Motor proteins. Cold Spring Harbor Perspect. . Biol. 10:a021931
    [Google Scholar]
  136. 136.
    Talbert PB, Masuelli R, Tyagi AP, Comai L, Henikoff S 2002. Centromeric localization and adaptive evolution of an Arabidopsis histone H3 variant. Plant Cell 14:1053–66
    [Google Scholar]
  137. 137.
    Tanenbaum ME, Macůrek L, Janssen A, Geers EF, Alvarez-Fernández M, Medema RH. 2009. Kif15 cooperates with Eg5 to promote bipolar spindle assembly. Curr. Biol. 19:1703–11
    [Google Scholar]
  138. 138.
    Tovey CA, Conduit PT. 2018. Microtubule nucleation by γ-tubulin complexes and beyond. Essays Biochem. 62:765–80
    [Google Scholar]
  139. 139.
    Twell D, Park SK, Hawkins TJ, Schubert D, Schmidt R et al. 2002. MOR1/GEM1 has an essential role in the plant-specific cytokinetic phragmoplast. Nat. Cell Biol. 4:711–14
    [Google Scholar]
  140. 140.
    Van Damme D, De Rybel B, Gudesblat G, Demidov D, Grunewald W et al. 2011. Arabidopsis α Aurora kinases function in formative cell division plane orientation. Plant Cell 23:4013–24
    [Google Scholar]
  141. 141.
    Vanstraelen M, Inzé D, Geelen D. 2006. Mitosis-specific kinesins in Arabidopsis. Trends Plant Sci. 11:167–75
    [Google Scholar]
  142. 142.
    Verdaasdonk JS, Bloom K. 2011. Centromeres: unique chromatin structures that drive chromosome segregation. Nat. Rev. Mol. Cell Biol. 12:320–32
    [Google Scholar]
  143. 143.
    Wadsworth P. 2015. TPX2. Curr. Biol. 25:R1156–58
    [Google Scholar]
  144. 144.
    Wadsworth P. 2021. The multifunctional spindle midzone in vertebrate cells at a glance. J. Cell Sci. 134:jcs250001
    [Google Scholar]
  145. 145.
    Walczak CE, Gayek S, Ohi R. 2013. Microtubule-depolymerizing kinesins. Annu. Rev. Cell Dev. Biol. 29:417–41
    [Google Scholar]
  146. 146.
    Wang C, Liu W, Wang G, Li J, Dong L et al. 2017. KTN80 confers precision to microtubule severing by specific targeting of katanin complexes in plant cells. EMBO J. 36:3435–47
    [Google Scholar]
  147. 147.
    Weimer AK, Demidov D, Lermontova I, Beeckman T, Van Damme D. 2016. Aurora kinases throughout plant development. Trends Plant Sci. 21:69–79
    [Google Scholar]
  148. 148.
    Weingartner M, Binarova P, Drykova D, Schweighofer A, David JP et al. 2001. Dynamic recruitment of Cdc2 to specific microtubule structures during mitosis. Plant Cell 13:1929–43
    [Google Scholar]
  149. 149.
    Wimbish RT, DeLuca JG. 2020. Hec1/Ndc80 tail domain function at the kinetochore-microtubule interface. Front. Cell Dev. Biol. 8:43
    [Google Scholar]
  150. 150.
    Wittmann T, Hyman A, Desai A 2001. The spindle: a dynamic assembly of microtubules and motors. Nat. Cell Biol. 3:E28–34
    [Google Scholar]
  151. 151.
    Wolniak SM, Hepler PK, Jackson WT. 1980. Detection of the membrane-calcium distribution during mitosis in Haemanthus endosperm with chlorotetracycline. J. Cell Biol. 87:23–32
    [Google Scholar]
  152. 152.
    Yamada M, Goshima G. 2017. Mitotic spindle assembly in land plants: molecules and mechanisms. Biology 6:6
    [Google Scholar]
  153. 153.
    Yu H-G, Muszynski MG, Dawe RK. 1999. The maize homologue of the cell cycle checkpoint protein MAD2 reveals kinetochore substructure and contrasting mitotic and meiotic localization patterns. J. Cell Biol. 145:425–35
    [Google Scholar]
  154. 154.
    Zeng CJT, Lee Y-RJ, Liu B. 2009. The WD40 repeat protein NEDD1 functions in microtubule organization during cell division in Arabidopsis thaliana. Plant Cell 21:1129–40
    [Google Scholar]
  155. 155.
    Zhang H, Deng X, Sun B, Van SL, Kang Z et al. 2018. Role of the BUB3 protein in phragmoplast microtubule reorganization during cytokinesis. Nat. Plants 4:485–94
    [Google Scholar]
/content/journals/10.1146/annurev-arplant-070721-084258
Loading
/content/journals/10.1146/annurev-arplant-070721-084258
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