, Volume 74, Issue 5, pp 555–562 | Cite as

Analysis of cytoskeleton in the cells involved in cytomixis: the migrated chromatin displays an MT-organizing activity and can interact with the spindle

  • Sergey R. MursalimovEmail author
  • Yuriy V. Sidorchuk
  • Elena V. Deineko
Original Article


The structure of cytoskeleton in the tobacco male meiocytes involved in the migration of nuclei between cells (cytomixis) is studied. The tubulin and actin components of cytoskeleton are examined using specific antibodies and phalloidin. The presence of microtubules and actin filaments inside cytomictic channels directly when the nuclei migrate through these channels is demonstrated for the first time. The actin and tubulin cytoskeleton is shown to retain its reticular structure in early prophase I before the beginning of cytomixis, during nuclear migration, and after completion of this process and emergence of micronuclei in the cytoplasm of recipient cells. It is demonstrated that if migration takes place in late prophase I, the nucleus leaves the perinuclear tubulin cage, encompassing it at this stage. After migration, the cytomictic micronuclei in recipient cell reside beyond the perinuclear tubulin cage in both meiotic prophase I and II. A microtubule-organizing activity of the migrated chromatin in meta-telophase I and II is demonstrated for the first time as well as the ability of this chromatin to form independent minispindles and radial microtubule arrays and contact the spindle of recipient cell. The role of cytomixis in production of aneuploid and unreduced pollen is discussed.


Micronuclei Meiosis Nuclear migration Minispindles Tubulin Unreduced pollen 



Cytomictic channels


Actin filaments




Microtubules stabilizing buffer


Ethylene glycol tetraacetic acid




1.4-piperazinediethane sulfonic acid


Fluorescein isothiocyanate


Perinuclear tubulin cage


Microtubule organizing centers



The work was supported by the Russian Foundation for Basic Research [16-34-60007 mol_a_dk] and Siberian Branch of the Russian Academy of Science under the program “Molecular genetic bases of regulation of genes expression, morphology, differentiation and cell reprogramming” [0324-2019-0042]. The authors thank Dr. Dmitri Demidov and Dr. Twan Rutten (IPK, Germany) for their assistances in the actin staining protocol development. The microscopy was conducted at the Joint Access Center for Microscopy of Biological Objects with the Siberian Branch of the Russian Academy of Sciences.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Barton DA, Cantrill LC, Law AMK et al (2014) Chilling to zero degrees disrupts pollen formation but not meiotic microtubule arrays in Triticum aestivum L. Plant Cell Environ 37:2781–2794. CrossRefGoogle Scholar
  2. Bone CR, Chang Y-T, Cain NE et al (2016) Nuclei migrate through constricted spaces using microtubule motors and actin networks in C. elegans hypodermal cells. Development 143:4193–4202. CrossRefGoogle Scholar
  3. Fakhri Z, Mirzaghaderi G, Ahmadian S, Mason AS (2016) Unreduced gamete formation in wheat × Aegilops spp. hybrids is genotype specific and prevented by shared homologous subgenomes. Plant Cell Rep 35:1143–1154. CrossRefGoogle Scholar
  4. Farooq U, Lovleen SMIS (2014) Male meiosis and behaviour of sex chromosomes in different populations of Rumex acetosa L. from the Western Himalayas, India. Plant Syst Evol 300:287–294. CrossRefGoogle Scholar
  5. Feijo JA, Pais MS (1989) Cytomixis in meiosis during the microsporogenesis of Ophrys lutea: an ultrastructural study. Caryologia 42:37–48. CrossRefGoogle Scholar
  6. Gupta RC, Goyal H, Singh V (2014) Cytology of the genus Artemisia (Anthemidae, Asteraceae) in the Western Himalayas. Biologia 69:1134–1141. CrossRefGoogle Scholar
  7. Kravets E, Yemets A, Blume Y (2017) Cytoskeleton and nucleoskeleton involvement in processes of cytomixis in plants. Cell Biol Int.
  8. Kumar S, Jeelani SM, Rani S et al (2013) Cytology of five species of subfamily Papaveroideae from the Western Himalayas. Protoplasma 250:307–316. CrossRefGoogle Scholar
  9. Lavia GI, Ortiz AM, Robledo G et al (2011) Origin of triploid Arachis pintoi (Leguminosae) by autopolyploidy evidenced by FISH and meiotic behaviour. Ann Bot 108:103–111. CrossRefGoogle Scholar
  10. Lone FA, Lone S (2013) Cytomixis – a well known but less understood phenomenon in plants. Int J Recent Sci Res 4:347–352Google Scholar
  11. Luo XJ, Liu XH, Wang CY, Wang XY (2008) Formation of membrane-bound inclusions and their associations with cytoplasmic channels in early prophase male meiocytes of Althaea rosea (L.) Cavan. Cell Biol Int 32:374–383. CrossRefGoogle Scholar
  12. Malik R, Gupta R, Singh V et al (2017) New chromosome reports in Lamiaceae of Kashmir (northwest Himalaya), India. Protoplasma 254:971–985. CrossRefGoogle Scholar
  13. Mandal A, Datta AK, Gupta S et al (2013) Cytomixis-a unique phenomenon in animal and plant. Protoplasma 250(5):985–996. CrossRefGoogle Scholar
  14. Meunier S, Vernos I (2016) Acentrosomal microtubule assembly in mitosis: the where, when, and how. Trends Cell Biol 26:80–87. CrossRefGoogle Scholar
  15. Mursalimov SR, Deineko EV (2012) An ultrastructural study of microsporogenesis in tobacco line SR1. Biologia 67:369–376. CrossRefGoogle Scholar
  16. Mursalimov SR, Deineko EV (2015) How cytomixis can form unreduced gametes in tobacco. Plant Syst Evol 301:1293–1297. CrossRefGoogle Scholar
  17. Mursalimov S, Deineko E (2018) Cytomixis in plants: facts and doubts. Protoplasma 255:719–731. CrossRefGoogle Scholar
  18. Mursalimov S, Permyakova N, Deineko E et al (2015) Cytomixis doesn’t induce obvious changes in chromatin modifications and programmed cell death in tobacco male meiocytes. Front Plant Sci 6:1–13. CrossRefGoogle Scholar
  19. Mursalimov S, Sidorchuk Y, Deineko E (2017) Behavior of nucleolus in the tobacco male meiocytes involved in cytomixis. Cell Biol Int 41(3):340–344. CrossRefGoogle Scholar
  20. Ogienko A, Karagodin D, Pavlova N et al (2008) Molecular and genetic description of a new hypomorphic mutation of Trithorax-like gene and analysis of its effect on Drosophila melanogaster oogenesis. Russ J Dev Biol 39:108–115CrossRefGoogle Scholar
  21. Pan Y, Wang X, Zheng G (2002) The arrangement of microtrabecular network during chromatin migration process and immunolocalization of actin and myosin in pollen mother cells of David lily. Caryologia 55:217–227. CrossRefGoogle Scholar
  22. Pécrix Y, Rallo G, Folzer H et al (2011) Polyploidization mechanisms: temperature environment can induce diploid gamete formation in Rosa sp. J Exp Bot 62:3587–3597. CrossRefGoogle Scholar
  23. Sidorchuk YV, Deineko EV, Shumny VK (2007a) Peculiarities of cytomixis in pollen mother cells of transgenic tobacco plants (Nicotiana tabacum L.) with mutant phenotype. Cell Tiss Biol 1:570–576. CrossRefGoogle Scholar
  24. Sidorchuk YV, Deineko EV, Shumny VK (2007b) Role of microtubular cytoskeleton and callose walls in the manifestation of cytomixis in pollen mother cells of tobacco Nicotiana tabacum L. Cell Tiss Biol 1:577–581. CrossRefGoogle Scholar
  25. Sidorchuk YV, Novikovskaya AA, Deineko EV (2016) Cytomixis in the cereal (Gramineae) microsporogenesis. Protoplasma 253:291–298. CrossRefGoogle Scholar
  26. Silkova OG, Shchapova AI, Shumny VK (2011) Patterns of meiosis in ABDR amphihaploids depend on the specific type of univalent chromosome division. Euphytica 178:415–426. CrossRefGoogle Scholar
  27. Singhal VK, Kumar P (2008) Impact of cytomixis on meiosis, pollen viability and pollen size in wild populations of Himalayan poppy (Meconopsis aculeata Royle). J Biosci 33:371–380CrossRefGoogle Scholar
  28. Sulimenko V, Hájková Z, Klebanovych A, Dráber P (2017) Regulation of microtubule nucleation mediated by γ-tubulin complexes. Protoplasma 254:1187–1199. CrossRefGoogle Scholar
  29. Tsvetova M, Elkonin L (2013) Cytological investigation of pollen development in Sorghum line with male sterility induced by sodium ascorbate in tissue culture. Am J Plant Sci 4:11–18. CrossRefGoogle Scholar
  30. Wang XY, Nie XW, Guo GQ et al (2002) Ultrastructural characterization of the cytoplasmic channel formation between pollen mother cells of David lily. Caryologia 55:161–169. CrossRefGoogle Scholar
  31. Wang XY, Yu CH, Li X et al (2004) Ultrastructural aspects and possible origin of cytomictic channels providing intercellular connection in vegetative tissues of anthers. Russ J Plant Physiol 51:110–120CrossRefGoogle Scholar
  32. Wang CY, Li X, Wu QF, Wang X (2006) Cytoplasmic channels and their association with plastids in male meiocytes of tobacco, onion and lily. Cell Biol Int 30:406–411. CrossRefGoogle Scholar
  33. Xu C, Liu Z, Zhang L et al (2013) Organization of actin cytoskeleton during meiosis I in a wheat thermo-sensitive genic male sterile line. Protoplasma 250:415–422. CrossRefGoogle Scholar
  34. Zhang WC, Yan WM, Lou CH (1985) Mechanism of intercellular movement of protoplasm in wheat nucellus. Sci China 28:1175–1187. Google Scholar
  35. Zhang WC, Yan WM, Lou CH (1990) Intercellular movement of protoplasm in vivo in developing endosperm of wheat caryopses. Protoplasma 153:193–203CrossRefGoogle Scholar

Copyright information

© Institute of Molecular Biology, Slovak Academy of Sciences 2019

Authors and Affiliations

  1. 1.Institute of Cytology and GeneticsRussian Academy of SciencesNovosibirskRussian Federation

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