Skip to main content
Log in

Morpho-Biological and Cytological Characterization of Tomato Roots (Solanum lycopersicum L., cv. Rekordsmen) Regenerated under NaCl Salinity in vitro

  • Published:
Cell and Tissue Biology Aims and scope Submit manuscript

Abstract

A comparative analysis of tomato roots regenerated in vitro on media supplemented with different NaCl concentrations (0–250 mM) has been carried out. A morphogenetic study performed at the organ level has determined rhizogenesis-inhibiting NaCl concentrations, while the morphometric analysis of regenerated roots in juvenile seedlings has registered such characteristics as their number, length, and fresh/dry weight. A cytological study has revealed some tissue disorders, such as changes in the vacuolization of root cap cells and root cortex cells (RCC) under salinity conditions. At some NaCl concentrations, significant changes in the cells of these tissues have been observed in relation to such parameters as the root cap length (50–100 and 250 mM NaCl), the number of root cap layers (50, 75, 150–250 mМ NaCl), the area of central cylinder cells (CCCs, 75–150 and 250 mM NaCl), the RCC area (100–200 mM NaCl), and the nucleolus to nucleus ratio (25, 50, and 200 mM NaCl). Using cytophotometry, we have shown there to be an increase in the number of interphase cells of the root meristem in the G2 phase with a simultaneous decrease of this parameter in the G1 phase. Immunofluorescent labeling has revealed various disorganizations in the alpha-tubulin cytoskeleton of interphase root meristem cells. Using transmission electron microscopy, we have revealed structural changes in plastids of root cap cells, RCC, and CCC, as well as changes in the organization of a nuclear compartment in RCC occurred in the presence of 150 mM NaCl. The studied characteristics can be used for a comparative evaluation of tomato genotypes under salinity at different levels of their organization. The proposed approach can be also used for crops that have no difficulties with induced rhizogenesis in vitro.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.
Fig. 7.
Fig. 8.
Fig. 9.

Similar content being viewed by others

REFERENCES

  1. Andronis, E.A. and Roubelakis-Angelakis, K.A., Short-term salinity stress in tobacco plants leads to the onset of animal-like PCD hallmarks in planta in contrast to long-term stress, Planta, 2010, vol. 231, pp. 437–448.

    Article  CAS  PubMed  Google Scholar 

  2. Armstrong, J.E. and Heimsch, C., Ontogenetic reorganization of the root meristem of Compositae, Am. J. Bot., 1976, vol. 63, pp. 212–219.

    Article  Google Scholar 

  3. Bagniewska-Zadworna, A. and Arasimowicz-Jelonek, M., The mystery of underground death: cell death in roots during ontogeny and in response to environmental factors, Plant Biol., 2016, vol. 18, pp. 171–184.

    Article  CAS  PubMed  Google Scholar 

  4. Bezrukova, M.V., Fatkhutdinova, R.A., and Shakirova, F.M., Protective effect of wheat germ agglutinin on the course of mitosis in the roots of Triticum aestivum seedlings exposed to cadmium. Russ. J. Plant Physiol., 2016, vol. 63, no. 3, pp. 358–364.

    Article  CAS  Google Scholar 

  5. Blancaflor, E.B. and Hasenstein, K.H., Growth and microtubule orientation of Zea mays roots subjected to osmotic stress, Int. J. Plant Sci., 1995, vol. 156, pp. 774–783.

    Article  CAS  PubMed  Google Scholar 

  6. Bogoutdinova, L.R., Baranova, G.B., Baranova, E.N., and Khaliluev, M.R., Comparative anatomical and morphological studies of the epidermal and cortical parenchyma hypocotyl cells of two tomato genotypes (Solanum lycopersicum L.) under sodium chloride stress in vitro, S.-Kh. Biol., 2016, vol. 51, no. 3, pp. 318–326.

    Google Scholar 

  7. Borek, S., Ratajczak, W., and Ratajczak, L., Ultrastructural and enzymatic research on the role of sucrose in mobilization of storage lipids in germinating yellow lupine seeds, Plant Sci., 2006, vol. 170, pp. 441–452.

    Article  CAS  Google Scholar 

  8. Burssens, S., Himanen, K., van, de, Cotte, B., Beeckman, T., Van, Montagu, M., Inzé, D., and Verbruggen, N., Expression of cell cycle regulatory genes and morphological alterations in response to salt stress in Arabidopsis thaliana,Planta, 2000, vol. 211, pp. 632–640.

    Article  CAS  PubMed  Google Scholar 

  9. Cano, E.A., Pérez-Alfocea, F., Moreno, V., Caro, M., and Bolarín, M.C., Evaluation of salt tolerance in cultivated and wild tomato species through in vitro shoot apex culture, Plant Cell Tiss. Org. Cult., 1998, vol. 53, pp. 19–26.

    Article  Google Scholar 

  10. Collings, D.A., Carter, C.N., Rink, J.C., Scott, A.C., Wayatt, S.E., and Stromgren-Allen, N., Plant nuclei can contain extensive grooves and invagination, Plant Cell, 2000, vol. 12, pp. 2425–2439.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Cuellar-Ortiz, S.M, De La Paz Arrieta-Montiel, M., Acosta-Gallegos, J., and Covarrubias, A.A., Relationship between carbohydrate partitioning and drought resistance in common bean, Plant Cell Environ., 2008, vol. 31, pp. 1399–1409.

    Article  PubMed  CAS  Google Scholar 

  12. Dhonukshe, P., Laxalt, A.M., Goedhart, J., Gadella, T.W.J., and Munnik, T., Phospholipase D activation correlates with microtubule reorganization in living plant cells, Plant Cell, 2003, vol. 15, pp. 2666–2679.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Ferdose, J., Kawasaki, M., Taniguchi, M., and Miyake, H., Differential sensitivity of rice cultivars to salinity and its relation to ion accumulation and root tip structure, Plant Prod. Sci., 2009, vol. 12, pp. 453–461.

    Article  CAS  Google Scholar 

  14. Francis, D., Kidd, A.D., and Bennett, M.D., DNA replication in relation to DNA C values, in The Cell Division Cycle Plants, Cambridge: Cambr. Univ. Press, 1985, pp. 61–82.

    Google Scholar 

  15. Gémes, K., Poór, P., Horváth, E., Kolbert, Z., Szopkó, D., Szepesi, A., and Tari, I., Cross-talk between salicylic acid and NaCl-generated reactive oxygen species and nitric oxide in tomato during acclimation to high salinity, Physiol. Plant., 2011, vol. 142, pp. 179–192.

    Article  PubMed  CAS  Google Scholar 

  16. González-Cruz, J. and Pastenes, C., Water-stress-induced thermotolerance of photosynthesis in bean (Phaseolus vulgaris L.) plants: the possible involvement of lipid composition and xanthophyll cycle pigments, Environ. Exp. Bot., 2012, vol. 77, pp. 127–140.

    Article  CAS  Google Scholar 

  17. Gudkov, I.N., Regulyatsiya fiziologicheskikh funktsii rastenii (Regulation of the Physiological Functions of Plants), Kiev: Naukova Dumka, 1986, pp. 18–30.

  18. Hajer, A.S., Malibari, A.A., Al-Zahrani, H.S., and Almaghrabi, O.A., Responses of three tomato cultivars to sea water salinity. 1. Effect of salinity on the seedling growth, Afr. J. Biotech., 2006, vol. 5, pp. 855–861.

    CAS  Google Scholar 

  19. Horie, T., Karahara, I., and Katsuhara, M., Salinity tolerance mechanisms in glycophytes: an overview with the central focus on rice plants, Rice, 2012, vol. 5, p. 11.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Huh, G.H., Damsz, B., Matsumoto, T.K., Reddy, M.P., Rus, A.M., Ibeas, J.I., Narasimhan, M.L., Bressan, R.A., and Hasegawa, P.M., Salt causes ion disequilibrium-induced programmed cell death in yeast and plants, Plant J., 2002, vol. 29, pp. 649–659.

    Article  CAS  PubMed  Google Scholar 

  21. Ivanov, V.B., Proliferatsiya kletok v rasteniyakh (Cell Proliferation in Plants), Itogi Nauki Tekhn., Ser. Tsitol., Moscow: VINITI., 1987, vol. 5.

  22. Ji, H., Pardo, J.M., Batelli, G., Van, Oosten, M.J., Bressan, R.A., and Li, X., The salt overly sensitive (SOS) pathway: established and emerging roles, Mol. Plant., 2013, vol. 6, pp. 275–286.

    Article  CAS  PubMed  Google Scholar 

  23. Kudoyarova, G.R., Kholodova, V.P., and Veselov, D.S., Current state of the problem of water relations in plants under water deficit, Russ. J. Plant Physiol., 2013, vol. 60, no. 2, pp. 165–175.

    Article  CAS  Google Scholar 

  24. Livanos, P., Galatis, B., Quader, H., and Apostolakos, P., Disturbance of reactive oxygen species homeostasis induces atypical tubulin polymer formation and affects mitosis in root-tip cells of Triticum turgidum and Arabidopsis thaliana,Cytoskeleton, 2012, vol. 69, pp. 1–21.

    Article  CAS  PubMed  Google Scholar 

  25. Lugan, R., Niogret, M.F., Leport, L., Guegan, J.P., Larher, F.R., Savoure, A., Kopka, J., and Bouchereau, A., Metabolome and water homeostasis analysis of Thellungiella salsuginea suggests that dehydration tolerance is a key response to osmotic stress in this halophyte, Plant J., 2010, vol. 64, pp. 215–229.

    Article  CAS  PubMed  Google Scholar 

  26. Meier, I., The plant nuclear envelope, Cell. Mol. Life Sci., 2001, vol. 58, pp. 1774–1780.

    Article  CAS  PubMed  Google Scholar 

  27. Mercado, J.A., Sancho-Carrascosa, M.A., Jimenez-Bermudes, S., Peran-Quesada, R., Pliego-Alfaro, F., and Quesada, M.A., Assessment of in vitro growth of apical stem sections and adventitious organogenesis to evaluate salinity tolerance in cultivated tomato, Plant Cell Tiss. Org. Cult., 2000, vol. 62, pp. 101–106.

    Article  Google Scholar 

  28. Mitsuya, S., Yamane, K., and Miyake, H.Takabe, T., Functional analysis of plasma membrane protein 3 (PMP3) homologs in salt tolerance of rice and Arabidopsis plants, in Proc. 2nd Int. Conf. Rice for the Future, Bangkok, Thailand, 2007, pp. 242–246.

  29. Mittova, V., Guy, M., Tal, M., and Volokita, M., Response of the cultivated tomato and its wild salt-tolerant relative Lycopersicon pennellii to salt-dependent oxidative stress: increased activities of antioxidant enzymes in root plastids, Free Radicals Res., 2002, vol. 36, pp. 195–202.

    Article  CAS  Google Scholar 

  30. Munns, R. and Tester, M., Mechanisms of salinity tolerance, Annu Rev. Plant Biol., 2008, vol. 59, pp. 651–681.

    Article  CAS  PubMed  Google Scholar 

  31. Murashige, T. and Skoog, F., A revised medium for rapid growth and bioassays with tobacco tissue culture, Physiol. Plant., 1962, vol. 15, pp. 473–497.

    Article  CAS  Google Scholar 

  32. Navrot, N., Rouhier, N., Gelhaye, E., and Jacquot, J.-P., Reactive oxygen species generation and antioxidant systems in plant mitochondria, Physiol. Plant., 2007, vol. 129, pp. 185–195.

    Article  CAS  Google Scholar 

  33. Park, H.J., Kim, W.Y., and Yun, D.J., A new insight of salt stress signaling in plant, Mol. Cells, 2016, vol. 39, pp. 447–459.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Peleg, Z., Apse, M., and Blumwald, E., Engineering salinity and water-stress tolerance in crop plants: getting closer to the field, Adv. Bot. Res., 2011, vol. 57, pp. 405–428.

    Article  CAS  Google Scholar 

  35. Pérez-Alfocea, F., Guerrier, G., Estañ, M.T., and Bolarin, M.C., Comparative salt responses at cell and whole-plant levels of cultivated and wild tomato species and their hybrid, J. Hort. Sci., 1994, vol. 69, pp. 639–644.

    Article  Google Scholar 

  36. Perilli, S., Di Mambro, R., and Sabatini, S., Growth and development of the root apical meristem, Curr. Opin. Plant Biol., 2012, vol. 15, pp. 17–23.

    Article  CAS  PubMed  Google Scholar 

  37. Reynolds, E.S., The use of lead citrate at high ph an electron-opaque stain in electron microscopy, J. Cell Biol., 1963, vol. 17, pp. 208–212.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Samarajeewa, P.K., Barrero, R.A., Umeda-Hara, C., Kawai, M., and Uchimiya, H., Cortical cell death, cell proliferation, macromolecular movements and RTip1 expression patterns in roots of rice (Oryza sativa L,) under NaCl stress, Planta, 1999, vol. 207, pp. 354–361.

    Article  CAS  Google Scholar 

  39. Serrano, R., Mulet, J., Rios, G., Marquez, J., de Larrinoa, I., Leube, M., Mendizabal, I., Pascual-Ahuir, A., Proft, M., Ros, R., and Montesinos, C., A glimpse of mechanisms of ion homeostasis during salt stress, J. Exp. Bot., 1999, vol. 50, pp. 1023–1036.

    Article  CAS  Google Scholar 

  40. Shibli, R.A., Kushad, M., Yousef, G.G., and Lila, M.A., Physiological and biochemical responses of tomato microshoots to induced salinity stress with associated ethylene accumulation, Plant Growth Reg., 2007, vol. 51, pp. 159–169.

    Article  CAS  Google Scholar 

  41. Strogonov, B.P., Structure and function of plant cells in saline habitats, in Israel Program for Scientific Translation, New York: Halstad Press, 1974.

    Google Scholar 

  42. Suzuki, N., Miller, G., Morales, J., Shulaev, V., Torres, M.A., and Mittler, R., Respiratory burst oxidases: the engines of ROS signaling, Curr. Opin. Plant Biol., 2011, vol. 14, pp. 691–699.

    Article  CAS  PubMed  Google Scholar 

  43. Tal, M., Salt tolerance in the wild relatives of the cultivated tomato: responses of Lycopersicon esculentum, L, peruvianum and L. esculentum minor to sodium chloride solution, Austr. J. Agric. Res., 1971, vol. 22, pp. 631–638.

    Article  CAS  Google Scholar 

  44. Teerarak, M., Bhinija, K., Thitavasanta, S., and Laosinwattana, C., The impact of sodium chloride on root growth, cell division, and interphase silver-stained nucleolar organizer regions (AgNORs) in root tip cells of Allium cepa L., Sci. Hort., 2009, vol. 121, pp. 228–232.

    Article  CAS  Google Scholar 

  45. Thuleau, P., Aldo, D., Cotelle, V., Brière, C., Ranty, B., Galaud, J.P., and Mazars, C., Relationships between calcium and sphingolipid-dependent signalling pathways during the early steps of plant–pathogen interactions, Bioch. Biophys. Acta., 2013, vol. 1833, pp. 1590–1594.

    Article  CAS  Google Scholar 

  46. Turhan, A., Şeniz, V., and Kuşçu, H., Genotypic variation in the response of tomato to salinity, Afr. J. Biotech., 2009, vol. 8, pp. 1062–1068.

    CAS  Google Scholar 

  47. Uzbekov, R.E., Analysis of protein expression level dynamics in the cell cycle using synchronized cells, Biochemistry (Moscow), 2004, vol. 69, no. 5, pp. 485–496.

    CAS  PubMed  Google Scholar 

  48. Wang, Y., Zhang, W., Li, K., Sun, F., Han, C., Wang, Y., and Li, X., Salt-induced plasticity of root hair development is caused by ion disequilibrium in Arabidopsis thaliana,J. Plant Res., 2008, vol. 121, pp. 87–96.

    Article  PubMed  Google Scholar 

  49. Wang, Y., Li, K., and Li, X., Auxin redistribution modulates plastic development of root system architecture under salt stress in Arabidopsis thaliana,J. Plant Physiol., 2009, vol. 166, pp. 1637–1645.

    Article  CAS  PubMed  Google Scholar 

  50. Wang, C., Zhang, L., Yuan, M., Y.Ge, Liu, Y., Fan, J., Ruan, Y., Cui, Z., Tong, S., and Zhang, S., The microfilament cytoskeleton plays a vital role in salt and osmotic stress tolerance in Arabidopsis,Plant Biol., 2010a, vol. 12, pp. 70–78.

    Article  PubMed  CAS  Google Scholar 

  51. Wang, J., Li, X, Liu, Y., and Zhao, X., Salt stress induces programmed cell death in Thellungiella halophila suspension-cultured cells, J. Plant Physiol., 2010b, vol. 167, pp. 1145–1151.

    Article  CAS  PubMed  Google Scholar 

  52. Weakley, B., A Beginner’s Handbook in Biological Electron Microscopy, Edinburgh: Churchill Livingstone, 1972.

    Google Scholar 

  53. West, G., Inze, D., and Beemster, G.T.S., Cell cycle modulation in the response of the primary root of Arabidopsis to salt stress, Plant Physiol., 2004, vol. 135, pp. 1050–1058.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Wood, D.E. and Newcomb, E.W., Caspase-dependent activation of calpain during drug-induced apoptosis, J. Biol. Chem., 1999, vol. 274, pp. 8309–8315.

    Article  CAS  PubMed  Google Scholar 

  55. Zhang, J.L. and Shi, H., Physiological and molecular mechanisms of plant salt tolerance, Photosynth. Res., 2013, vol. 115, pp. 1–22.

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This study was performed within the framework of state order no. 0574-2019-0002, АААА-А17-117030110149-8.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to L. R. Bogoutdinova.

Ethics declarations

The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

Additional information

Translated by N. Statsyuk

Abbreviations: ROS, reactive oxygen species; IBA, 3-indolebutyric acid; MS, Murashige and Skoog medium; RCC, root cortex cell; CCC, central cylinder cell; PCD, programmed cell death.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bogoutdinova, L.R., Baranova, E.N., Baranova, G.B. et al. Morpho-Biological and Cytological Characterization of Tomato Roots (Solanum lycopersicum L., cv. Rekordsmen) Regenerated under NaCl Salinity in vitro. Cell Tiss. Biol. 14, 228–242 (2020). https://doi.org/10.1134/S1990519X20030025

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1990519X20030025

Keywords:

Navigation