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Cellular mechanisms of nuclear migration

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Abstract

Subcellular mobility, positioning, and directional movement of the nucleus in a certain site of the cell or cenocyte and, less frequently, intercellular translocation of the nucleus accompany the cell and tissue differentiation, change of their functions, and the organism growth and development and its response to stress, plant–microbial interactions, symbiosis, and many other processes in plants and animals. The nucleus movement is performed and directed through the interaction between dynamic cytoskeleton components and nucleus by means of signal-binding proteins, including motor and linker. The cell responds to the external signal by mobilization and polar reconstruction of the cytoskeleton components, as a result of which the nucleus displacement by means of actomyosin or microtubule mechanisms in cooperation with dynein and kinesin occurs. In plants, the actomyosin mechanism is involved in the nucleus migration; it allows the nucleus to move rapidly and over significant distances in response to environmental stimuli. An important role in the nucleus translocation belongs to the linker complexes of the proteins that are inserted in the nuclear envelope, that connect and transmit signals from the plasmalemma to the cytoplasm and nucleoplasm, and that provide the skeletal basis for many subcellular compartments. Changes in the protein composition, conformational modifications of the proteins, and displacement of linkers from the nuclear envelope result in the nucleus detachment from the cytoskeleton, and change in the form, mechanical rigidity, and positioning of the nucleus.

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References

  1. Starr, D.A. and Fridolfsson, H.N, Interactions between nuclei and the cytoskeleton are mediated by SUN-KASH nuclear-envelope bridges, Annu. Rev. Cell Dev. Biol., 2010, vol. 26, pp. 421–444.

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Starr, D.A., A nuclear-envelope bridge positions nuclei and moves chromosomes, J. Cell Sci., 2009, vol. 122, no. 5, pp. 577–586.

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Hetzer, M.W, The nuclear envelope, Cold Spring Harb. Persp. Biol., 2010, vol. 2, no. 3, p. a000539.

    Google Scholar 

  4. Peremyslov, V.V., Mockler, T.C., Filichkin, S.A., Fox, S.E., Jaiswal, P., Makarova, K.S., Koonin, E.V., and Dolja, V.V, Expression, splicing, and evolution of the myosin gene family in plants, Plant Physiol., 2011, vol. 155, no. 3, pp. 1191–1204.

    CAS  PubMed  Google Scholar 

  5. Tamura, K., Iwabuchi, K., Fukao, Y., Kondo, M., Okamoto, K., Ueda, H., Nishimura, M., and Hara-Nishimura, I, Myosin XI-i links the nuclear membrane to the cytoskeleton to control nuclear movement and shape in Arabidopsis, Curr. Biol., 2013, vol. 23, no. 18, pp. 1776–1781.

    CAS  PubMed  Google Scholar 

  6. Griffis, A.H.N., Groves, N.R., Zhou, X., and Meier, I, Nuclei in motion: movement and position of plant nuclei in development, signaling, symbiosis, and disease, Front. Plant Sci., 2014, vol. 5, p. 129.

    Google Scholar 

  7. Zhou, X., Graumann, K., Evans, D.E., and Meier, I, Novel plant sun-kash bridges are involved in rangap anchoring and nuclear shape determination, J. Cell Biol., 2012, vol. 196, no. 2, pp. 203–211.

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Zhou, X., Graumann, K., Wirthmueller, L., Jones, J.D.G., and Meier, I, Identification of unique sun-interacting nuclear envelope proteins with diverse functions in plants, J. Cell Biol., 2014, vol. 205, no. 5, pp. 677–692.

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Friedl, P., Wolf, K., and Lammerding, J, Nuclear mechanics during cell migration, Curr. Opin. Cell Biol., 2011, vol. 23, no. 1, pp. 55–64.

    CAS  PubMed  Google Scholar 

  10. Wu, J., Lee, K.C., Dickinson, R.B., and Lele, T.P, How dynein and microtubules rotate the nucleus, J. Cell Physiol., 2011, vol. 226, no. 10, pp. 2666–2674.

    CAS  PubMed  Google Scholar 

  11. Wu, J., Kent, I.A., Shekhar, N., Chancellor, T.J., Mendonca, A., Dickinson, R.B., and Lele, T.P, Actomyosin pulls to advance the nucleus in a migrating tissue cell, Biophys. J., 2014, vol. 106, no. 1, pp. 7–15.

    PubMed  PubMed Central  Google Scholar 

  12. Gundersen, G.G. and Worman, H.J, Nuclear positioning, Cell, 2013, vol. 152, no. 6, pp. 1376–1389.

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Russell, S.D, Double fertilization, Int. Rev. Cytol., 1992, vol. 140, pp. 357–388.

    Google Scholar 

  14. Koltzov, N.K. Organisation of Cell, Moscow, 1936.

    Google Scholar 

  15. Raftopoulou, M. and Hall, A, Cell migration: Rho GTPases lead the way, Dev. Biol., 2004, vol. 265, no. 1, pp. 23–32.

    CAS  PubMed  Google Scholar 

  16. Li, J., Xu, Y., and Chong, K, The novel functions of kinesin motor proteins in plants, Protoplasma, 2012, vol. 249, no. 2, pp. 95–100.

    CAS  Google Scholar 

  17. Applewhite, D.A., Grode, K.D., Keller, D., Zadeh, A.D., Sle, K.C., and Rogers, S.L, The spectraplakin short stop is an actin-microtubule cross-linker that contributes to organization of the microtubule network, Mol. Biol. Cell, 2010, vol. 21, no. 10, pp. 1714–1724.

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Kodama, A., Lechler, T., and Fuchs, E, Coordinating cytoskeletal tracks to polarize cellular movements, J. Cell Biol., 2004, vol. 167, no. 2, pp. 203–207.

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Xiang, X. and Fischer, R, Nuclear migration and positioning in filamentous fungi, Fungal Genet. Biol., 2004, vol. 41, no. 4, pp. 411–419.

    CAS  PubMed  Google Scholar 

  20. Gladfelter, A. and Berman, J, Dancing genomes: fungal nuclear positioning, Nat. Rev. Microbiol., 2009, vol. 7, no. 12, pp. 875–886.

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Gibeaux, R. and Knop, M, When yeast cells meet, karyogamy! An example of nuclear migration slowly resolved, Nucleus, 2013, vol. 4, no. 3, pp. 182–188.

    PubMed  Google Scholar 

  22. Reinsch, S. and Gonczy, P, Mechanisms of nuclear positioning, J. Cell Sci., 1998, vol. 111, no. 16, pp. 2283–2295.

    CAS  PubMed  Google Scholar 

  23. Ohnishi, Yu., Hoshino, R., and Takashi, O, Dynamics of male and female chromatin during karyogamy in rice zygotes, Plant Physiol., 2014, vol. 165, no. 4, pp. 1533–1543.

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Luxton, G.W. and Gundersen, G.G, Orientation and function of the nuclear-centrosomal axis during cell migration, Curr. Opin. Cell Biol., 2011, vol. 23, no. 5, pp. 579–588.

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Kirschner, M. and Mitchison, T, Beyond self-assembly: from microtubules to morphogenesis, Cell, 1986, vol. 45, no. 3, pp. 329–342.

    CAS  PubMed  Google Scholar 

  26. Mimori-Kiyosue, Y. and Tsukita, S., “Search-andcapture” of microtubules through plus-end-binding proteins (+TIPs), J. Biochem., 2003, vol. 134, no. 3, pp. 321–326.

    CAS  PubMed  Google Scholar 

  27. Galjart, N, Clips and clasps and cellular dynamics, Nat. Rev. Mol. Cell Biol., 2005, vol. 6, no. 6, pp. 487–498.

    CAS  PubMed  Google Scholar 

  28. Mallik, R. and Gross, S.P, Molecular motors: strategies to get along, Curr. Biol., 2004, vol. 14, no. 22, pp. 971–982.

    Google Scholar 

  29. Oh, S.A., Pal, M.D., Park, S.K., Johnson, J.A., and Twell, D, The tobacco MAP215/Dis1-family protein TMBP200 is required for the functional organization of microtubule arrays during male germ-line establishment, J. Exp. Bot., 2010, vol. 61, no. 4, pp. 969–981.

    CAS  PubMed  Google Scholar 

  30. Park, S.K., Howden, R., and Twell, D, The Arabidopsis thaliana gametophytic mutation gemini pollen1 disrupts microspore polarity, division asymmetry and pollen cell fate, Development, 1998, vol. 125, no. 19, pp. 3789–3799.

    CAS  PubMed  Google Scholar 

  31. Twell, D., Park, S.K., Hawkins, T.J., Schubert, D., Schmidt, R., Smertenko, A., and Hussey, P.J., MOR1/GEM1 plays an essential role in the plant-specific cytokinetic phragmoplast, Nat. Cell Biol., 2002, vol. 4, no. 9, pp. 711–714.

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Astrom, H., Sorri, O., and Raudaskoski, M, Role of microtubules in the movement of the vegetative nucleus and generative cell in tobacco pollen tubes, Sex. Plant Reprod., 1995, vol. 8, no. 2, pp. 61–69.

    Google Scholar 

  33. Heslop-Harrison, J., Heslop-Harrison, Y., Cresti, M., Tiezzi, A., and Moscatelli, A, Cytoskeletal elements, cell shaping and movement in the angiosperm pollen tube, J. Cell Sci., 1988, vol. 91, pp. 49–60.

    Google Scholar 

  34. Bibikova, T.N., Blancaflor, E.B., and Gilroy, S, Microtubules regulate tip growth and orientation in root hairs of Arabidopsis thaliana, Plant J., 1999, vol. 17, no. 6, pp. 657–665.

    CAS  PubMed  Google Scholar 

  35. Moscatelli, A., Del Casino, C., Lozzi, L., Cai, G., Scali, M., Tiezzi, A., and Cresti, M, High molecular weight polypeptides related to dynein heavy chains in Nicotiana tabacum pollen tubes, J. Cell Sci., 1995, vol. 108, no. 3, pp. 1117–1125.

    CAS  PubMed  Google Scholar 

  36. Lawrence, C.J., Morris, N.R., Meagher, R.B., and Dawe, R.K, Dyneins have run their course in plant lineage, Traffic, 2001, vol. 2, no. 5, pp. 362–363.

    CAS  PubMed  Google Scholar 

  37. Lambert, A.M., Microtubule-organizing centers in higher plants, Curr. Opin. Cell Biol., 1993, vol. 5, no. 1, pp. 116–122.

    CAS  PubMed  Google Scholar 

  38. Shamina, N.V., Shatskaia, O.A., Solov’eva, N.V., and Blinova, E.A, Polyarchal spindles in higher plant meiosis, Tsitologiia, 2006, vol. 48, no. 2, pp. 114–119.

    CAS  PubMed  Google Scholar 

  39. Shamina, N.V., Zaporozhchenko, I.A., Maksiutova, Y.R., and Shatskaia, O.A, Cortical cytoskeletal ring in prophase II leads to correction of abnormalities of the first meiotic division and to meiotic restitution of pollen mother cell nucleus, Tsitologiia, 2007, vol. 49, no. 10, pp. 865–869.

    CAS  PubMed  Google Scholar 

  40. Chaffey, N, The plant cytoskeleton in cell differentiation and development, Ann. Bot., 2005, vol. 95, no. 7, pp. 1253–1254.

    PubMed Central  Google Scholar 

  41. Higaki, T., Sano, T., and Hasezawa, S, Actin microfilament dynamics and actin side-binding proteins in plants, Curr. Opin. Plant Biol., 2007, vol. 10, no. 6, pp. 549–556.

    CAS  PubMed  Google Scholar 

  42. Tominaga, M., Kojima, H., Yokota, E., Orii, H., Nakamori, R., Katayama, E., Anson, M., Shimmen, T., and Oiwa, K, Higher plant myosin XImoves processively on actin with 35 nm steps at high velocity, EMBO J., 2003, vol. 22, no. 6, pp. 1263–1272.

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Heslop-Harrison, J., Heslop-harrisony. conformation and movement of the vegetative nucleus of the angiosperm pollen tube: association with the actin cytoskeleton, J. Cell Sci., 1989, vol. 93, pp. 299–308.

    Google Scholar 

  44. Gorshkova, T.A., Plant Cell Wall as a Dynamic System, Moscow: Science, 2007.

    Google Scholar 

  45. Collings, D.A. and Wasteneys, G.O, Actin microfilament and microtubule distribution patterns in the expanding root of Arabidopsis thaliana, Can. J. Bot., 2005, vol. 83, no. 6, pp. 579–590.

    Google Scholar 

  46. Lee, S.H. and Dominguez, R, Regulation of actin cytoskeleton dynamics in cells, Mol. Cells, 2010, vol. 29, no. 4, pp. 311–325.

    CAS  PubMed  Google Scholar 

  47. Peremyslov, V.V., Klocko, A.L., Fowler, J.E., and Dolja, V.V, Arabidopsis myosin XI-K localizes to the motile endomembrane vesicles associated with F-actin, Front. Plant Sci., 2012, vol. 3, p. 184.

    PubMed  PubMed Central  Google Scholar 

  48. Cai, N., Henty-Ridilla, J.L., Szymanski, D.B., and Staiger, C.J, Arabidopsis myosin XI: a motor rules the tracks, Plant Physiol., 2014, vol. 166, no. 3, pp. 1359–1370.

    PubMed  PubMed Central  Google Scholar 

  49. Pollard, T.D. and Borisy, G.G, Cellular motility driven by assembly and disassembly of actin filaments, Cell, 2003, vol. 112, no. 4, pp. 453–465.

    CAS  PubMed  Google Scholar 

  50. Rouiller, I., Xu, X.-P., Amann, K.J., Egile, C., Nickell, S., Nicastro, D., Li, R., Pollard, T.D., Volkmann, N., and Hanein, D, The structural basis of actin filament branching by the Arp2/3 complex, J. Cell Biol., 2008, vol. 180, no. 5, pp. 887–895.

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Firat-Karalar, E.N. and Welch, M.D, New mechanisms and functions of actin nucleation, Curr. Opin. Cell Biol., 2011, vol. 23, no. 1, pp. 4–13.

    CAS  PubMed  Google Scholar 

  52. Khatau, S.B., Hale, C.M., Stewart-Hutchinson, P.J., Patel, M.S., Stewart, C.L., Searson, P.C., Hodzic, D., and Wirtz, D., A perinuclear actin cap regulates nuclear shape, Proc. Natl. Acad. Sci. U. S. A., 2009, vol. 106, no. 45, pp. 19017–19022.

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Khatau, S.B., Bloom, R.J., Bajpai, S., Razafsky, D., Zang, S., Giri, A., Wu, P.H., Marchand, J., Ce-ledon, A., Hale, C.M., Sun, S.X., Hodzic, D., and Wirtz, D, The distinct roles of the nucleus and nucleus-cytoskeleton connections in three-dimensional cell migration, Sci. Rep., 2012, vol. 2, art. no. 488.

    PubMed  PubMed Central  Google Scholar 

  54. Wang, X.Y., Nie, X.W., Guo, G.Q., Pan, Y.F., and Zheng, G.C, Ultrastructural characterization of the cytoplasmic channel formation between pollen mother cells of David lily, Caryologia, 2002, vol. 55, no. 2, pp. 161–169.

    Google Scholar 

  55. Walpita, D. and Hay, E, Studying actin-dependent processes in tissue culture, Nat. Rev. Mol. Cell Biol., 2002, vol. 3, no. 2, pp. 137–141.

    CAS  PubMed  Google Scholar 

  56. Cramer, L.P, Forming the cell rear first: breaking cell symmetry to trigger directed cell migration, Nat. Cell Biol., 2010, vol. 12, no. 7, pp. 628–632.

    CAS  PubMed  Google Scholar 

  57. Martini, F.J. and Valdeolmillos, M., Actomyosin contraction at the cell rear drives nuclear translocation in migrating cortical interneurons, J. Neurosci., 2010, vol. 30, no. 25, pp. 8660–8670.

    CAS  PubMed  Google Scholar 

  58. Suozzi, K.C., Wu, X., and Fuchs, E, Spectraplakins: master orchestrators of cytoskeletal dynamics, J. Cell Biol., 2012, vol. 197, no. 4, pp. 465–475.

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Wittmann, T. and Waterman-Storer, C.M, Cell motility: can Rho GTPases and microtubules point the way?, J. Cell Sci., 2001, vol. 114, pp. 3795–3803.

    CAS  PubMed  Google Scholar 

  60. Wehrle-Haller, B. and Imhof, B.A, Actin, microtubules and focal adhesion dynamics during cell migration, Int. J. Biochem. Cell Biol., 2003, vol. 35, no. 1, pp. 39–50.

    CAS  PubMed  Google Scholar 

  61. Subramanian, A., Prokop, A., Yamamoto, M., Sugimura, K., Uemura, T., Betschinger, J., Knoblich, J.A., and Volk, T, Shortstop recruits EB1/APC1 and promotes microtubule assembly at the muscle-tendon junction, Curr. Biol., 2003, vol. 13, no. 13, pp. 1086–1095.

    CAS  PubMed  Google Scholar 

  62. Roper, K. and Brown, N.H, Maintaining epithelial integrity: a function for gigantic spectraplakin isoforms in adherens junctions, J. Cell Biol., 2003, vol. 162, no. 7, pp. 1305–1315.

    PubMed  PubMed Central  Google Scholar 

  63. Sonnenberg, A. and Liem, R.K, Plakins in development and disease, Exp. Cell Res., 2007, vol. 313, no. 10, pp. 2189–2203.

    CAS  PubMed  Google Scholar 

  64. Buey, R.M., Mohan, R., Leslie, K., Walzthoeni, T., Missimer, J.H., Menzel, A., Bjelic, S., Bargsten, K., Grigoriev, I., Smal, I., Meijering, E., Aebersold, R., Akhmanova, A., and Steinmetz, M.O, Insights into EB1 structure and the role of its C-terminal domain for discriminating microtubule tips from the lattice, Mol. Biol. Cell, 2011, vol. 22, no. 16, pp. 2912–2923.

    CAS  PubMed  PubMed Central  Google Scholar 

  65. Feijo, J.A. and Pais, M.S, Cytomixis in meiosis during the microsporogenesis of Ophrys lutea: an ultrastructural study, Caryologia, 1989, vol. 42, no. 1, pp. 37–48.

    Google Scholar 

  66. Shamina, N.V., Dorogova, N.V., Zagorskaya, A.A., Deineko, E.V., and Shumnyi, V.K, Disruption of male meiosis in transgenic tobacco lines res91, Cell Tissue Biol., 2000, vol. 42, no. 12, pp. 1159–1164.

    CAS  Google Scholar 

  67. Zhang, Q., Ragnauth, C., Greener, M.J., Shanahan, C.M., and Roberts, R.G, The nesprins are giant actin-binding proteins, orthologous to Drosophila melanogaster muscle protein MSP-300, Genomics, 2002, vol. 80, no. 5, pp. 473–481.

    CAS  PubMed  Google Scholar 

  68. Mellad, J.A., Warren, D.T., and Shanahan, C.M, Nesprins LINC the nucleus and cytoskeleton, Curr. Opin. Cell Biol., 2011, vol. 23, no. 1, pp. 47–54.

    CAS  PubMed  Google Scholar 

  69. Evans, D.E., Pawar, V., Smith, S.J., and Graumann, K, Protein interactions at the higher plant nuclear envelope: evidence for a linker of nucleoskeleton and cytoskeleton complex, Front Plant Sci., 2014, vol. 5, no. 183, pp. 1–5.

    Google Scholar 

  70. Mislow, J.M., Kim, M.S., Davis, D.B., and McNally, E.M., Myne-1, a spectrin repeat transmembrane protein of the myocyte inner nuclear membrane, interacts with lamin A/C, J. Cell Sci., 2002, vol. 115, pp. 61–70.

    CAS  PubMed  Google Scholar 

  71. Zhen, Y.Y., Libotte, T., Munck, M., Noegel, A.A., and Korenbaum, E, Nuance,a giant protein connecting the nucleus and actin cytoskeleton, J. Cell Sci., 2002, vol. 115, pp. 3207–3222.

    CAS  PubMed  Google Scholar 

  72. Pershina, E.G., Morozova, K.N., and Kiseleva, E.V., Nesprins—nuclear envelope proteins ensuring integrity, Cell Tissue Biol., 2014, vol. 56, no. 7, pp. 467–479.

    CAS  Google Scholar 

  73. Starr, D.A. and Han, M, Role of ANC-1 in tethering nuclei to the actin cytoskeleton, Science, 2002, vol. 298, no. 5592, pp. 406–409.

    CAS  PubMed  Google Scholar 

  74. Rajgor, D. and Shanahan, C.M, Nesprins: from the nuclear envelope and beyond, Exp. Rev. Mol. Med., 2013, vol. 15, p. e5. doi doi 10.1017/erm.2013.6

    Google Scholar 

  75. Padmakumar, V.C., Libotte, T., Lu, W., Zaim, H., Abraham, S., Noegel, A.A., Gotzmann, J., Foisner, R., and Karakesisoglou, I, The inner nuclear membrane protein Sun1 mediates the anchorage of Nesprin-2 to the nuclear envelope, J. Cell Sci., 2005, vol. 118, no. 15, pp. 3419–3430.

    CAS  PubMed  Google Scholar 

  76. Naismith, T.V., Heuser, J.E., Breakefield, X.O., and Hanson, P.I, Torsin A in the nuclear envelope, Proc. Natl. Acad. Sci. U. S. A., 2004, vol. 101, no. 20, pp. 7612–7617.

    CAS  PubMed  PubMed Central  Google Scholar 

  77. Nery, F.C., Zeng, J., Niland, B.P., Hewett, J., Farley, J., Irimia, D., Li, Y., Wiche, G., Sonnenberg, A., and Breakefield, X.O., Torsin A binds the KASH domain of nesprins and participates in linkage between nuclear envelope and cytoskeleton, J. Cell Sci., 2008, vol. 121, pp. 3476–3486.

    CAS  PubMed  Google Scholar 

  78. Malik, P., Zuleger, N., and Schirmer, E.C, Nuclear envelope influences on genome organization, Biochem. Soc. Trans., 2010, vol. 38, pp. 268–272.

    CAS  PubMed  Google Scholar 

  79. Lei, K., Zhu, X., Xu, R., Shao, C., Xu, T., Zhuang, Y., and Han, M, Inner nuclear envelope proteins SUN1 and SUN2 play a prominent role in the DNA damage response, Curr. Biol., 2012, vol. 22, no. 17, pp. 1609–1615.

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Chytilova, E., Macas, J., Sliwinska, E., Rafelski, S.M., Lambert, G.M., and Galbraith, D.W, Nuclear dynamics in, Arabidopsis thaliana, Mol. Biol. Cell, 2000, vol. 11, no. 8, pp. 2733–2741.

    CAS  PubMed  Google Scholar 

  81. Ueda, H., Yokota, E., Kutsuna, N., Shimada, T., Tamura, K., Shimmen, T., Hasezawa, S., Dolja, V.V., and Hara-Nishimura, I., Myosin-dependent endoplasmic reticulum motility and f-actin organization in plant cells, Proc. Natl. Acad. Sci. U. S. A., 2010, vol. 107, no. 15, pp. 6894–6899.

    CAS  PubMed  PubMed Central  Google Scholar 

  82. Zickler, D. and Kleckner, N, The leptotene-zygotene transition of meiosis, Ann. Rev. Genet., 1998, vol. 32, pp. 619–697.

    CAS  PubMed  Google Scholar 

  83. Murphy, S.P., Gumber, H.K., Mao, Y., and Bass, H.W., A dynamic meiotic SUN belt includes the zygotenestage telomere bouquet and is disrupted in chromosome segregation mutants of maize (Zea mays L.), Front. Plant. Sci., 2014, vol. 5, no. 314, pp. 1–10.

    CAS  Google Scholar 

  84. Tomita, K. and Cooper, J.P, The telomere bouquet controls the meiotic spindle, Cell, 2007, vol. 130, no. 1, pp. 113–126.

    CAS  PubMed  Google Scholar 

  85. Chikashige, Y., Tsutsumi, C., Yamane, M., Okamasa, K., Haraguchi, T., and Hiraoka, Y, Meiotic proteins bqt1 and bqt2 tether telomeres to form the bouquet arrangement of chromosomes, Cell, 2006, vol. 125, no. 1, pp. 59–69.

    CAS  PubMed  Google Scholar 

  86. Yamamoto, A., West, R.R., McIntosh, J.R., and Hiraoka, Y., A cytoplasmic dynein heavy chain is required for oscillatory nuclear movement of meiotic prophase and efficient meiotic recombination in fission yeast, J. Cell Biol., 1999, vol. 145, no. 6, pp. 1233–1249.

    CAS  PubMed  PubMed Central  Google Scholar 

  87. Koszul, R., Kim, K.P., Prentiss, M., Kleckner, N., and Kameoka, S, Meiotic chromosomes move by linkage to dynamic actin cables with transduction of force through the nuclear envelope, Cell, 2008, vol. 133, no. 7, pp. 1188–1201.

    CAS  PubMed  PubMed Central  Google Scholar 

  88. Ohkura, H, Meiosis: an overview of key differences from mitosis, Cold Spring Harbor Persp. Biol., 2015, vol. 7, no. 5, p. a015859.

    Google Scholar 

  89. Mursalimov, S., Sidorchuk, Yu., Baiborodin, S., and Deineko, E, Distribution of telomeres in the tobacco meiotic nuclei during cytomixis, Cell Biol. Int., 2015, vol. 39, no. 4, pp. 491–495.

    CAS  PubMed  Google Scholar 

  90. Mursalimov, S., Permyakova, N., Deineko, E., Houben, A., and Demidov, D, Cytomixis doesn’t induce obvious changes in chromatin modifications and programmed cell death in tobacco male meiocytes, Front. Plant Sci., 2015, vol. 6, art. no. 846. doi 10.3389/ fpls.2015.00846

  91. Yang, J., Yu, C.H., Wang, X.Y., and Zheng, G.C, Ultrastructural observation on the intra and intercellular microtrabecular network of the pollen mother cells in onion (Allium cepa), Acta Bot. Sin., 2001, vol. 43, no. 4, pp. 331–338.

    Google Scholar 

  92. Yang, J., Peng, Z.-S., Li, W., Gao, H.-H., and Zheng, G.-C., Ultrastructural observation on the cellular skeleton during cytomixis in pollen mother cells of tabacco (Nicotiana tabacum), Acta Bot. Yunnanica, 2004, vol. 26, no. 3, pp. 329–333.

    Google Scholar 

  93. Pan, Y.F., Wang, X.Y., Zheng, G.C., and Cheng, K.C, The arrangement of microtrabecular network during chromatin migration process and immunolocalization of actin and myosin in pollen mother cells of David lily, Caryologia, 2002, vol. 55, no. 3, pp. 217–227.

    Google Scholar 

  94. Mursalimov, S.R. and Deineko, E.V, An ultra-structural study of microsporogenesis in tobacco line SR1, Biologia, 2012, vol. 67, no. 3, pp. 369–376.

    CAS  Google Scholar 

  95. Sydorchuk, Yu.V., Kravets, E.A., Mursalimov, S.R., Plohovskaya, S.G., Goryunov, I.I., Yemets, A.I., Blume, Ya.B., and Deyneko, E.V, Evaluation of the use of temperature stress for induction cytomixis in microsporogenesis of dicotyledonous (N. tabacum L.) and monocotyledonous (H. distichum L.) plants, Russ. J. Dev. Biol., 2016, vol. 47, no. 6, pp. 1–16.

    Google Scholar 

  96. Kravets, E.A., Sidorchuk, Yu.V., Horyunova, I.I., Plohovskaya, S.G., Mursalimov, S.R., Deineko, E.V., Yemets, A.I., and Blume, Ya.B., Intra- and intertissular cytomictic interactions in the microsporogenesis of mono- and dicotyledonous plants, Cytol. Genet., 2016, vol. 50, no. 5, pp. 267–277.

    Google Scholar 

  97. Mursalimov, S.R., Baiborodin, S.I., Sidorchuk, Yu.V., Shumny, V.K., and Deineko, E.V, Characteristics of the cytomictic channel formation in Nicotiana tabacum L. pollen mother cells, Cytol. Genet., 2010, vol. 44, no. 1, pp. 14–18.

    Google Scholar 

  98. Mursalimov, S.R., Sidorchuk, Y.V., and Deineko, E.V, New insights into cytomixis: specific cellular features and prevalence in higher plants, Planta, 2013, vol. 238, no. 3, pp. 415–423.

    CAS  PubMed  Google Scholar 

  99. Sidorchuk, Y.V., Novikovskaya, A.A., and Deineko, E.V, Cytomixis in the cereal (Gramineae) microsporogenesis, Protoplasma, 2015, vol. 253, no. 2, pp. 291–298.

    PubMed  Google Scholar 

  100. Zhang, W.C., Yan, W.M., and Lou, C.H, Mechanism of intercellular movement of protoplasm in wheat nucellus, Sci. China, 1985, vol. 28, no. 11, pp. 1175–1187.

    Google Scholar 

  101. Zhang, W.C, Progress in research on intercellular movement of protoplasm in higher plants, Acta Bot. Sin., 2002, vol. 44, no. 9, pp. 1068–1074.

    CAS  Google Scholar 

  102. Wang, Y.X., Nie, X.W., and Zheng, G.C, The effects of cytochalasin b on chromatin movement through cell wall, Chin. Bull. Bot., 1984, vol. 2, pp. 39–41.

    Google Scholar 

  103. Sidorchuk, Yu.V., Deineko, E.V., and Shumny, V.K, The role of microtubular cytoskeleton and callose walls in the cytomixis process in tobacco (Nicotiana tabacum L.) pollen mother cells, Cell Tissue Biol., 2007, vol. 49, no. 10, pp. 876–880.

    Google Scholar 

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Authors and Affiliations

  1. Institute of Food Biotechnology and Genomics, National Academy of Sciences of Ukraine, Kyiv, Ukraine

    E. A. Kravets, A. I. Yemets & Ya. B. Blume

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  1. E. A. Kravets
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  2. A. I. Yemets
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  3. Ya. B. Blume
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Correspondence to E. A. Kravets.

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Original Russian Text © E.A. Kravets, A.I. Yemets, Ya.B. Blume, 2017, published in Tsitologiya i Genetika, 2017, Vol. 51, No. 3, pp. 54–65.

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Kravets, E.A., Yemets, A.I. & Blume, Y.B. Cellular mechanisms of nuclear migration. Cytol. Genet. 51, 192–201 (2017). https://doi.org/10.3103/S0095452717030069

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