Skip to main content
SpringerLink
Log in

Involvement of plant cytoskeleton in cellular mechanisms of metal toxicity

  • Published:
Cytology and Genetics Aims and scope Submit manuscript

Abstract

Literature data and results of the studies carried out us concerning the involvement of plant cell cytoskeleton in cellular mechanisms of metal toxicity are summarized. Characteristics of cytotoxic effect of metals on plant cytoskeleton and, in particular, on microtubules and actin filaments are reviewed. Particular attention is paid to cellular and molecular mechanisms of metal impact on cytoskeleton. The most probable binding sites of heavy metals, as well as alternative mechanisms of their impact on cytoskeleton, are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Duffus, J.H., “Heavy metals”—a meaningless term?, Pure Appl. Chem., 2002, vol. 74, no. 5, pp. 793–807.

    Article  CAS  Google Scholar 

  2. Jadia, C.D. and Fulekar, M.H., Phytoremediation of heavy metals: recent techniques, Afr. J. Biotechnol., 2009, vol. 8, no. 6, pp. 921–928.

    CAS  Google Scholar 

  3. Ghosh, M. and Singh, S.P., A review on phytoremediation of heavy metals and utilization of its byproduct, Appl. Ecol. Environ. Res., 2005, vol. 3, no. 1, pp. 1–18.

    Article  Google Scholar 

  4. Wierzbicka, M., Przedpelska, E., Ruzik, R., Ouerdane, L., Povec-Pawlak, K., Jarosz, M., Szpunar, J., and Szakiel, A., Comparison of the toxicity and distribution of cadmium and lead in plant cells, Protoplasma, 2007, vol. 231, pp. 99–111.

    Article  CAS  PubMed  Google Scholar 

  5. Liliom, K., Wagner, G., Pacz, A., Cascante, M., Kovacs, J., and Ovadi, J., Organization-dependent effects of toxic bivalent ions. Microtubule assembly and glycolysis, Eur. J. Biochem., 2000, vol. 267, pp. 473–479.

    Article  Google Scholar 

  6. Meharg, A.A. and Macnair, M.R., An altered phosphate uptake system in arsenate-tolerant Holcus lanatus, New Phytol., 1990, vol. 116, pp. 29–35.

    Article  CAS  Google Scholar 

  7. Krzeslowska, M., The cell wall in plant cell response to trace metals: polysaccharide remodeling and its role in defense strategy, Acta Physiol. Plant., 2011, vol. 33, pp. 35–51.

    Article  CAS  Google Scholar 

  8. Ehrhardt, D.W. and Shaw, S.L., Microtubule dynamics and organization in the plant cortical array, Annu. Rev. Plant Biol., 2006, vol. 57, pp. 859–875.

    Article  CAS  PubMed  Google Scholar 

  9. Nick, P., Microtubules as sensors for abiotic stimuli, in Plant Microtubules. Development and Flexibility, Nick, P., Ed., Berlin, Heidelberg: Springer-Verlag, 2008, pp. 175–206.

    Chapter  Google Scholar 

  10. Blume, Ya.B., Krasylenko, Yu.A., and Yemets, A.I., Effects of phytohormones on the cytoskeleton of the plant cell, Russ. J. Plant Physiol., 2012, vol. 59, no. 4, pp. 515–529.

    Article  CAS  Google Scholar 

  11. Yemets, A.I., Krasylenko, Y.A., Lytvyn, D.I., Sheremet, Ya.A., and Blume, Ya.B., Nitric oxide signalling via cytoskeleton in plants, Plant Sci., 2011, vol. 181, pp. 545–554.

    Article  CAS  PubMed  Google Scholar 

  12. Nagle, A., Hur, W., and Gray, N.S., Antimitotic agents of natural origin, Curr. Drug Targets, 2006, vol. 7, pp. 305–326.

    Article  CAS  PubMed  Google Scholar 

  13. Pribyl, P., Cepák, V., and Zachleder, V., Cytoskeletal alterations in interphase cells of the green alga Spirogyra decimina in response to heavy metals exposure: I. The effect of cadmium, Protoplasma, 2005, vol. 226, pp. 231–240.

    Article  CAS  PubMed  Google Scholar 

  14. Heng, Y.W. and Koh, Ch.-G., Actin cytoskeleton dynamics and the cell division cycle, Int. J. Biochem. Cell Biol., 2010, vol. 42, pp. 1622–1633.

    Article  CAS  PubMed  Google Scholar 

  15. Schmidt, S.M. and Panstruga, R., Cytoskeleton functions in plant-microbe interactions, Physiol. Mol. Plant Pathol., 2007, vol. 71, pp. 135–148.

    Article  CAS  Google Scholar 

  16. Song, X., Ma, Q., Hao, X., and Li, H., Roles of the actin cytoskeleton and an actin-binding protein in wheat resistance against Puccinia striiformis f. sp. tritici, Protoplasma, 2012, vol. 249, pp. 99–106.

    Article  CAS  PubMed  Google Scholar 

  17. Komis, G., Apostolakos, P., and Galatis, B., Hyperosmotic stress-induct actin filaments reorganization in leaf cells of Chlorophiton comosoum, J. Exp. Bot., 2002, vol. 53, no. 375, pp. 1699–1710.

    Article  CAS  PubMed  Google Scholar 

  18. Shibasaki, K., Uemura, M., Tsurumi, S., and Rahman, A., Auxin response in Arabidopsis under cold stress: underlying molecular mechanisms, Plant Cell, 2009, vol. 21, pp. 3823–3838.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  19. Yamamoto, K. and Kiss, J.Z., Disruption of the actin cytoskeleton results in the promotion of gravitropism in inflorescence stems and hypocotyls of Arabidopsis, Plant Physiol., 2002, vol. 128, pp. 669–681.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  20. Veseleska, R. and Janisch, R., The effect of UV irradiation on changes in cytoskeleton and viability of mouse fibroblasts L929 cell line, Scripta Medica (BRNO), 2000, vol. 73, no. 6, pp. 393–408.

    Google Scholar 

  21. Grzanka, D., Domaniewski, J., Grzanka, A., and Zuryn, A., Ultraviolet radiation (UV) induces reorganization of actin cytoskeleton in CHOAA8 cells, Neoplasma, 2006, vol. 53, pp. 328–332.

    CAS  PubMed  Google Scholar 

  22. Cooper, J.A., Effects of cytochalasin and phalloidin on actin, J. Cell Biol., 1987, vol. 105, pp. 1473–1478.

    Article  CAS  PubMed  Google Scholar 

  23. Dudás, R., Kupi, T., Vig, A., Orbán, J., and Lrinczy, D., Effect of phalloidin on the skeletal muscle ADF-actin filaments, J. Trans. Am. Stud., 2009, vol. 95, pp. 709–712.

    Google Scholar 

  24. Omata, W., Shibata, H., Li, L., Takata, K., and Kojima, I., Actin filaments play a critical role in insulin-induced exocytotic recruitment but not in endocytosis of GLUT4 in isolated rat adipocytes, Biochem. J., 2000, vol. 346, pp. 321–328.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  25. Chen, T., Teng, N., Wu, X., Wang, Y., Tang, W., Samaj, J., Baluska, F., and Lin, J., Disruption of actin filaments by latrunculin B affects cell wall construction in Picea meyeri pollen tube by disturbing vesicle trafficking, Plant Cell Physiol., 2007, vol. 48, no. 1, pp. 19–30.

    Article  CAS  PubMed  Google Scholar 

  26. Liu, D., Jiang, W., and Gao, X., Effects of cadmium on root growth, cell division and nucleoli in root tip cells of garlic, Biol. Plant., 2003/2004, vol. 47, pp. 79–83.

    Article  Google Scholar 

  27. Fusconi, A., Gallo, C., and Camusso, W., Effects of cadmium on root apical meristems of Pisum sativum L. cell viability, cell proliferation and microtubule pattern as suitable markers for assessment of stress pollution, Mutat. Res., 2007, vol. 632, pp. 9–19.

    Article  CAS  PubMed  Google Scholar 

  28. Dong, J., Mao, W.H., Zhang, G.P., and Wu, F.B., Cail, Y., Root excretion and plant tolerance to cadmium toxicity—a review, Plant Soil Environ., 2007, vol. 53, no. 5, pp. 193–200.

    CAS  Google Scholar 

  29. Parween, T., Jan, S., Sharma, M.P.M., Mujib, A., and Fatma, T., Genotoxic impact of cadmium on root meristem of Vicia faba L., Russ. Agricult. Sci., 2011, vol. 37, pp. 115–119.

    Article  Google Scholar 

  30. Boominathan, P. and Doran, P., Cadmium tolerance and antioxidative defenses in hairy roots of the cadmium hyperaccumulator, Thlaspi caerulescens, Biotech. Bioeng., 2003, vol. 83, no. 2, pp. 158–167.

    Article  CAS  Google Scholar 

  31. Fan, J.-L., Wei, X.-G., Wan, L.-C., Zhang, L.-Y., Zhao, X.-Q., Liu, W.-Z., Hao, H.-Q., and Zhang, H.-Y., Disarrangement of actin filaments and Ca2+ gradient by CdCl2 alters cell wall construction in Arabidopsis thaliana root hairs by inhibiting vesicular trafficking, J. Plant Physiol., 2011, vol. 168, pp. 1157–1167.

    Article  CAS  PubMed  Google Scholar 

  32. Horiunova, I.I., Krasylenko, Ya.A., Zaslavsky, V.A., and Yemets, A.I., Cadmium effect’s on the organization of actin filaments in Arabidopsis thaliana roots cells, Dopov. Nac. Akad. Nauk Ukr., 2014, vol. 9, pp. 127–133.

    Google Scholar 

  33. Liu, D.H., Jiang, W.S., and Li, M.X., Effects of Cd2+ on root growth and cell division of Allium cepa L., Acta Sci. Circumstantiae, 1992, vol. 12, no. 4, pp. 439–446.

    CAS  Google Scholar 

  34. Liu, D., Jiang, W., and Gao, X., Effects of cadmium on root growth, cell division and nucleoli in root tip cells of garlic, Biol. Plant., 2003/2004, vol. 47, pp. 79–83.

    Article  Google Scholar 

  35. Siddiqui, S., Meghvansi, M.K., Wani, M.A., and Jabee, F., Evaluating cadmium toxicity in the root meristem of Pisum sativum L., Acta Physiol. Plant., 2009, vol. 31, pp. 531–536.

    Article  CAS  Google Scholar 

  36. Bandyopadhyay, D., Chatterjee, A.K., and Datta, A.G., Effect of cadmium on purified hepatic flavokinase: involvement of reactive SH group(s) in the inactivation of flavokinase by cadmium, Life Sci., 1997, vol. 60, pp. 1891–1903.

    Article  CAS  PubMed  Google Scholar 

  37. Dovgalyuk, A., Kalynyak, T., and Blume, Ya.B., Heavy metals have a different action from aluminium in disrupting microtubules in Allium cepa L. meristematic cells, Cell Biol. Int., 2003, vol. 27, pp. 193–195.

    Article  CAS  PubMed  Google Scholar 

  38. Xu, P., Liu, D., and Jiang, W., Cadmium effects on the organization of microtubular cytoskeleton in interphase and mitotic cells of Allium sativum, Biol. Plant., 2009, vol. 53, no. 2, pp. 387–390.

    Article  CAS  Google Scholar 

  39. Wallin, M. and Hartley-Asp, B., Effects of potential aneuploidy inducing agents on microtubule assembly in vitro, Mutat. Res., 1993, vol. 287, pp. 17–22.

    Article  CAS  PubMed  Google Scholar 

  40. Díaz-Barriga, F., Carrizalaens, L., and Yanez, L., Interaction of cadmium with actin microfilaments in vitro, Toxicol. In Vitro, 1989, vol. 3, no. 4, pp. 277–284.

    Article  PubMed  Google Scholar 

  41. Buljan, V., Yeung, S., Rushdi, S., Delikatny, E.J., and Hambly, B., Mercury and cadmium effects on microtubule polymerisation and depolymerisation, Biophys. J., 2001, vol. 80, p. 99.

    Google Scholar 

  42. Perrino, B.A. and Chou, I.-N., Role of calmodulin in cadmium-induced microtubule disassembly, Cell Biol. Int. Rep., 1986, vol. 10, no. 7, pp. 565–573.

    Article  CAS  PubMed  Google Scholar 

  43. Cheung, W.Y., Calmodulin: its potential role in cell proliferation and heavy metal toxicity, Fed. Proc., 1984, vol. 43, no. 15, pp. 2995–2999.

    CAS  PubMed  Google Scholar 

  44. Soetan, K.O., Olaiya, C.O., and Oyewol, O.E., The importance of mineral elements for humans, domestic animals and plants: a review, Afr. Food Sci., 2010, vol. 4, no. 5, pp. 200–222.

    CAS  Google Scholar 

  45. Piechalaka, A., Tomaszewskaa, B., Baralkiewiczb, D., and Maleckaa, A., Accumulation and detoxification of lead ions in legumes, Phytochemistry, 2002, vol. 60, pp. 153–162.

    Article  Google Scholar 

  46. Jiang, W. and Liu, D., Effects of Pb21 on root growth, cell division, and nucleolus of Zea mays L., Bull. Environ. Contam. Toxicol., 2000, vol. 65, pp. 786–793.

    Article  CAS  PubMed  Google Scholar 

  47. Wierzbicka, M., The effect of lead on the cell cycle in the root meristem of Allium cepa L., Protoplasma, 1999, vol. 207, pp. 186–194.

    Article  CAS  Google Scholar 

  48. Liu, D.H., Xue, P., Meng, Q., Zhe, J., Gu, J., and Jiang, W., Pb/Cu effects on the organization of microtubule cytoskeleton in interphase and mitotic cells of Allium sativum L., Plant. Cell. Rep., 2009, vol. 28, pp. 695–702.

    Article  CAS  PubMed  Google Scholar 

  49. Their, R., Bonacker, D., Stoiber, T., Böhm, K.J., Wang, M., Unger, E., Bolt, H.M., and Degen, G., Interaction of metal salts with cytoskeletal motor protein systems, Toxicol. Lett., 2003, vols. 140–141, pp. 75–81.

    Article  Google Scholar 

  50. Bonacker, D., Stoiber, T., Böhm, K.J., Prots, I., Wang, M., Unger, E., Their, R., Bolt, H.M., and Degen, G.H., Genotoxicity of inorganic lead salts and disturbance of microtubule function, Environ. Mol. Mutagen., 2005, vol. 45, pp. 346–353.

    Article  CAS  PubMed  Google Scholar 

  51. Faulstich, H., Stournaras, C., Doenges, K.H., and Zimmermann, H.-P., The molecular mechanism of interaction of EtsPb+ with tubulin, FEBS Lett., 1984, vol. 174, no. 1, pp. 128–131.

    Article  CAS  PubMed  Google Scholar 

  52. Zimmermann, H.P., Faulstich, H., Hansch, G.M., Doenges, K.H., and Stournaras, C., The interaction of triethyl lead with tubulin and microtubules, Mutat. Res., 1988, vol. 201, pp. 293–302.

    Article  CAS  PubMed  Google Scholar 

  53. Jan, A.T., Murtaza, I., Ali, A., Mohd, Q., and Haq, R., Mercury pollution: an emerging problem and potential bacterial remediation strategies, World J. Microbiol. Biotech., 2009, vol. 25, no. 9, pp. 1529–1537.

    Article  CAS  Google Scholar 

  54. Kaivalya, M., Nageshwar,Rao B.N., and Satish, Rao B.S., Mangiferin: a xanthone attenuates mercury chloride induced cytotoxicity and genotoxicity in HepG2 cells, J. Biochem. Mol. Toxicol., 2011, vol. 25, no. 2, pp. 108–116.

    Article  CAS  PubMed  Google Scholar 

  55. Blamey, F.P.C., Kopittke, P.M., Wehr, J.B., and Menzies, N.W., Recovery of cowpea seedling roots from exposure to toxic concentrations of trace, Plant Soil, 2011, vol. 341, pp. 423–436.

    Article  CAS  Google Scholar 

  56. Wallin, M., Larrson, H., and Edstrom, A., Tubulin sulfhydryl groups and polymerization in vitro. Effects of diand trivalent cations, Exp. Cell Res., 1977, vol. 107, pp. 219–225.

    Article  CAS  PubMed  Google Scholar 

  57. Vogel, D.G., Margolis, R.L., and Mottet, N.K., The effects of methyl mercury binding to microtubules, Toxicol. Appl. Pharmacol., 1985, vol. 80, pp. 473–486.

    Article  CAS  PubMed  Google Scholar 

  58. Vogel, D.G., Margolis, R.L., and Mottet, N.K., Analysis of methyl mercury binding sites on tubulin subunits and microtubules, BMC Pharmacol. Toxicol., 1989, vol. 64, pp. 196–201.

    Article  CAS  Google Scholar 

  59. Kennedy, A.J., Johnson, D.R., Seiter, J.M., Lindsay, J.H., Boyd, R.E., Bednar, A.J., and Allison, P., Tungsten toxicity, bioaccumulation and compartmentalization into organisms representing two trophic levels, Environ. Sci. Technol., 2012, vol. 46, no. 17, pp. 9646–9652.

    Article  CAS  PubMed  Google Scholar 

  60. Adamakis, I.-D.S., Panteris, E., and Eleftheriou, E.P., The fatal effect of tungsten on Pisum sativum L. root cells: indications for endoplasmic reticulum stressinduced programmed cell death, Planta, 2011, vol. 234, pp. 21–34.

    Article  CAS  PubMed  Google Scholar 

  61. Adamakis, I.-D.S., Panteris, E., and Eleftheriou, E.P., The cortical microtubules are a universal target of tungsten toxicity among land plant taxa, J. Biol Res., 2010, vol. 13, pp. 59–66.

    CAS  Google Scholar 

  62. Chen, C., Huang, D., and Liu, J., Functions and toxicity of nickel in plants: recent advances and future prospects, Clean, 2009, vol. 37, nos. 4–5, pp. 304–313.

    CAS  Google Scholar 

  63. Horiunova, I.I., Krasylenko, Ya., and Yemets, A.I., Nickel effect’s on the organization of actin filaments in arabidopsis thaliana roots cells, Dopov. Nac. Akad. Nauk Ukr., 2015, vol. 1, pp. 21–28.

    Google Scholar 

  64. Li, W., Zhao, Y., and Chou, I.-N., Nickel (Ni2+) enhancement of β-tubulin acetylation in cultured 3T3 cells, Toxicol. Appl. Pharmacol., 1996, vol. 140, pp. 461–470.

    Article  CAS  PubMed  Google Scholar 

  65. Li, W., Zhao, Y., and Chou, I.-N., (Ni2+) enhancement of microtubule assembly in vitro is dependent on GTP function, Toxicol. Appl. Pharmacol., 2003, vol. 193, pp. 202–208.

    Article  CAS  PubMed  Google Scholar 

  66. Marcano, L., Carruyo, I., Fernandez, Y., Montiel, X., and Torrebla, Z., Determination of vanadium accumulation in onion root cells (Allium cepa L.) and its correlation with toxicity, Biocell, 2006, vol. 30, no. 2, pp. 259–267.

    CAS  PubMed  Google Scholar 

  67. Rivadeneira, J., Barrio, D., Arrambide, G., Gambino, D., Bruzzone, L., and Etcheverry, S., Biological effects of a complex of vanadium (V) with salicylaldehyde semicarbazone in osteoblasts in culture: mechanism of action, J. Inorgan. Biochem., 2009, vol. 103, pp. 633–642.

    Article  CAS  Google Scholar 

  68. Ramirez, P., Eastmond, D.A., Laclette, J.P., and Ostrosky-Wegman, P., Disruption of microtubule assembly and spindle formation as a mechanism for the induction of aneuploid cells by sodium arsenite and vanadium pentoxide, Mutat. Res., 1997, vol. 386, pp. 29l–298.

    Article  Google Scholar 

  69. Ramos, S., Mouraa, J.J.G., and Aureliano, M., Recent advances into vanadyl, vanadate and decavanadate interactions with actin, Metallomics, 2012, vol. 4, pp. 16–22.

    Article  CAS  PubMed  Google Scholar 

  70. Eleftheriou, E.P., Adamakis, I.-D.S., and Melissa, P., Effects of hexavalent chromium on microtubule organization, ER distribution and callose deposition in root tip cells of Allium cepa L., Protoplasma, 2011, vol. 249, no. 2, pp. 401–416.

    Article  PubMed  Google Scholar 

  71. Fasulo, M., Bassi, M., and Domini, A., Cytotoxic effects of hexavalent chromium in Euglena gracilis: first observations, Protoplasma, 1982, vol. 110, pp. 39–47.

    Article  CAS  Google Scholar 

  72. Zou, J.H., Wang, M., Jiang, W.S., and Liu, D.H., Effects of hexavalent chromium (VI) on root growth and cell division in root tip cells of Amarantus viridis L., Pak. J. Bot., 2006, vol. 38, no. 3, pp. 673–681.

    Google Scholar 

  73. Eleftheriou, E.P., Adamakis, I.D., and Michalopoulou, V.A., Hexavalent chromium-induced differential disruption of cortical microtubules in some Fabaceae species is correlated with acetylation of β-tubulin, Protoplasma, 2015. DOI 10.1007.s00709-015-0831-4

    Google Scholar 

  74. Malerba, M., Crosti, P., and Cerana, P., Effect of heat stress on actin cytoskeleton and endoplasmic reticulum of tobacco BY-2 cultured cells and its inhibition by Co2+, Protoplasma, 2010, vol. 239, pp. 23–30.

    Article  CAS  PubMed  Google Scholar 

  75. Hutchins, B.M., Hancock, W.O., and Williams, M.E., Magnet assisted fabrication of microtubule arrays, Phys. Chem. Chem. Phys., 2006, vol. 8, pp. 3507–3509.

    Article  CAS  PubMed  Google Scholar 

  76. van de Mortel, J.E., Almar Villanueva, L., Schat, H., Kwekkeboom, J., Coughlan, S., Moerland, P.D., Ver Loren van Themaat, E., Koornneef, M., and Aarts, M.G.M., Large expression differences in genes for iron and zinc homeostasis, stress response, and lignin biosynthesis distinguish roots of Arabidopsis thaliana and the related metal hyperaccumulator, Thlaspi caerulescens, Plant Phys., 2006, vol. 142, pp. 1127–1147.

    Article  Google Scholar 

  77. Urnov, F.D., Rebar, E.J., Holmes, M.C., Zhang, H.S., and Gregory, P.D., Genome editing with engineered zinc finger nucleases, Nat. Rev. Genet., 2010, vol. 11, pp. 636–646.

    Article  CAS  PubMed  Google Scholar 

  78. Chang, H.-B., Lin, Ch.-W., and Huang, H.-J., Zincinduced cell death in rice (Oryza sativa L.) roots, Plant Growth Regul., 2005, vol. 46, pp. 261–266.

    Article  CAS  Google Scholar 

  79. Andriolia, N.B., Soloneskib, S., Larramendyb, M.L., and Mudrya, M.D., Cytogenetic and microtubule array effects of the zineb-containing commercial fungicide formulation Azzurro on meristematic root cells of Allium cepa L., Mutat. Res., 2012, vol. 742, pp. 48–53.

    Article  Google Scholar 

  80. Hesketh, J.E., Microtubule assembly in rat brain extracts. further characterization of the effects of zinc on assembly and cold stability, Int. J. Biol. Chem., 1984, vol. 16, no. 12, pp. 1331–1339.

    CAS  Google Scholar 

  81. Gaskin, F. and Kress, Y., Zinc ion-induced assembly of tubulin, J. Biol. Chem., 1977, vol. 252, no. 19, pp. 6918–6924.

    CAS  PubMed  Google Scholar 

  82. Eagle, G.R., Zombola, R.R., and Himes, R.H., Tubulin–zinc interactions: binding and polymerization studies, BMC Biochem., 1983, vol. 22, pp. 221–228.

    Article  CAS  Google Scholar 

  83. Lowe, J., Li, H., Downing, K.H., and Nogales, E., Refined structure of α-, β-tubulin at 3.5 Å resolution, J. Mol. Biol., 2001, vol. 313, pp. 1045–1057.

    Article  CAS  PubMed  Google Scholar 

  84. Camakaris, J., Voskoboinik, I., and Mercer, J.F., Molecular mechanism of copper homeostasis, Biochem. Biophys. Res. Commun., 1999, vol. 261, no. 2, pp. 225–232.

    Article  CAS  PubMed  Google Scholar 

  85. Liu, D.H., Xue, P., Meng, Q., Zhe, J., Gu, J., and Jiang, W., Pb/Cu effects on the organization of microtubule cytoskeleton in interphase and mitotic cells of Allium sativum L., Plant. Cell. Rep., 2009, vol. 28, pp. 695–702.

    Article  CAS  PubMed  Google Scholar 

  86. Kulikova, A.L., Kholodova, V.P., and Kuznetsov, V.V., Actin is involved in early plant responses to heavy metal stress and associates with molecular chaperons in stress environments, Russ. J. Rep. Dev. Biol. Sci., 2009, vol. 424, pp. 49–52.

    CAS  Google Scholar 

  87. Horiunova, I.I. and Yemets, A.I., Effect copper on actin filaments organization in Arabidopsis thaliana root cells, Fakt. Eksp. Evol. Organ., 2015, vol. 16, pp. 41–45.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Food Biotechnology and Genomics, National Academy of Sciences of Ukraine, Kyiv, 04123, Ukraine

    I. I. Horiunova, Yu. A. Krasylenko, A. I. Yemets & Ya. B. Blume

Authors
  1. I. I. Horiunova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yu. A. Krasylenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. I. Yemets
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ya. B. Blume
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ya. B. Blume.

Additional information

Original Russian Text © I.I. Horiunova, Yu.A. Krasylenko, A.I. Yemets, Ya.B. Blume, 2016, published in Tsitologiya i Genetika, 2016, Vol. 50, No. 1, pp. 57–67.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Horiunova, I.I., Krasylenko, Y.A., Yemets, A.I. et al. Involvement of plant cytoskeleton in cellular mechanisms of metal toxicity. Cytol. Genet. 50, 47–59 (2016). https://doi.org/10.3103/S0095452716010060

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.3103/S0095452716010060

Keywords

Search

Navigation