Skip to main content
SpringerLink
Log in

Cadmium toxicity and its relationship with disturbances in the cytoskeleton, cell cycle and chromosome stability

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

This study aimed to investigate the mode of action of cadmium (Cd) toxicity at cell level, especially at early stages of plant exposure. Tomato seedlings were cultivated in growth media containing from 0.1 to 70 µM CdCl2 for 24 h. Mitotic index, chromosome abnormality, DNA integrity and organization of tubulin-based structures were assessed in root cells. As higher the Cd concentration in the growth media, higher was the DNA damage intensity and the occurrence of chromosomal abnormalities that included chromosome lost, bridges, stickiness, C-metaphase and polyploidy. The profile of chromosomal aberrations also varied with elevated Cd concentration, being observed increases in the frequency of chromosome stickiness. The mitotic index was reduced at the lowest Cd concentration, but such reduction was statistically similar to that detected at the highest concentration, suggesting that mitotic depression is a rapid outcome and, at same time, a Cd-induced effect that is limited at the first 24 h of direct root exposure to this metal. Under exposure to 20 µM CdCl2, heterogenous distribution of the spindle fibers, formation of two spindle complexes in both of the cell poles, absence of centrosome center, polarization of the spindle fibers during cell division, and non-uniform tubulin deposition in microtubule and phragmoplast were noticed. The results indicate that the tubulin-dependent components of cytoskeleton are Cd targets, and the sensitivity of tubulin-based structures to Cd exposure depends on cell cycle phase. Moreover, DNA damage intensity and chromosomal abnormality profile can be employed as markers of Cd toxicity level.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Abdalla KO, Thomson JA, Rafudeen MS (2009) Protocols for nuclei isolation and nuclear protein extraction from the resurrection plant Xerophyta viscosa for proteomic studies. Anal Biochem 384:365–367

    CAS  Google Scholar 

  • Alves LA, Monteiro CC, Carvalho RF, Ribeiro PC, Tezotto T, Azevedo RA, Gratão PL (2017) Cadmium stress related to root-to-shoot communication depends on ethylene and auxin in tomato plants. Environ Exp Bot 134:102–115

    CAS  Google Scholar 

  • Araújo RP, Almeida A-AF, Pereira LS, Mangabeira PAO, Souza JO, Pirovani CP, Ahnert D, Baligar VC (2017) Photosynthetic, antioxidative, molecular and ultrastructural responses of young cacao plants to Cd toxicity in the soil. Ecotoxicol Environ Saf 144:148–157

    Google Scholar 

  • Arya SK, Mukherjee A (2014) Sensitivity of Allium cepa and Vicia faba towards cadmium toxicity. J Soil Sci Plant Nutr 14:447–458

    CAS  Google Scholar 

  • Avila-Ospina L, Moison M, Yoshimoto K, Daubresse CM (2014) Autophagy, plant senescence, and nutrient recycling. J Exp Bot 65:3799–811

    Google Scholar 

  • Bandyopadhyay A, Mukherjee A (2011) Sensitivity of Allium and Nicotiana in cellular and acellular comet assays to assess differential genotoxicity of direct and indirect acting mutagens. Ecotoxicol Environ Saf 74:860–865

    CAS  Google Scholar 

  • Bayçu G, Gevrek-Kürüm N, Moustaka J, Csatári I, Rognes SE, Moustakas M (2017) Cadmium-zinc accumulation and photosystem II responses of Noccaea caerulescens to Cd and Zn exposure. Environ Sci Pollut Res Int 24:2840–2850

    Google Scholar 

  • Borges KLR, Hippler FWR, Carvalho MEA, Nalin RS, Matias FI, Azevedo RA (2019) Nutritional status and root morphology of tomato under Cd-induced stress: comparing contrasting genotypes for metal-tolerance. Sci Hortic 246:518–527

    CAS  Google Scholar 

  • Borges KLR, Salvato F, Alcântara BK, Nalin RS, Piotto FA, Azevedo RA (2018) Temporal dynamic responses of roots in contrasting tomato genotypes to cadmium tolerance. Ecotoxicology 27:245–258

    CAS  Google Scholar 

  • Cabral Pinto MMS, Marinho-Reis AP, Almeida A, Ordens CM, Silva MMVG, Freitas S, Simões MR, Moreira PI, Dinis PA, Diniz ML, Ferreira da Silva EA, Condesso de Melo MT (2017) Human predisposition to cognitive impairment and its relation with environmental exposure to potentially toxic elements. Environ Geochem Health 40:1767–1784

    Google Scholar 

  • Carvalho MEA, Piotto FA, Franco MR, Borges KLR, Gaziola SA, Castro PRC, Azevedo RA (2018c) Cadmium toxicity degree on tomato development is associated with disbalances in B and Mn status at early stages of plant exposure. Ecotoxicology 27:1293–1302

    CAS  Google Scholar 

  • Carvalho MEA, Piotto FA, Franco MR, Martinelli AP, Cuypers A, Azevedo RA (2019) Relationship between Mg, B and Mn status and tomato tolerance against Cd toxicity. J Environ Manag 240:84–92

    CAS  Google Scholar 

  • Carvalho MEA, Piotto FA, Gaziola SA, Jacomino AP, Jozefczak M, Cuypers A, Azevedo RA (2018a) New insights about cadmium impacts on tomato: plant acclimation, nutritional changes, fruit quality and yield. Food Energy Secur 7:e00131

    Google Scholar 

  • Carvalho MEA, Piotto FA, Nogueira ML, Gomes-Junior FG, Chamma HMCP, Pizzaia D, Azevedo RA (2018b) Cadmium exposure triggers genotype-dependent changes in seed vigor and germination of tomato offspring. Protoplasma 255:989–999

    CAS  Google Scholar 

  • Cerda H, Delincée H, Haine H, Rupp H (1997) The DNA ‘comet assay’ as a rapid screening technique to control irradiated food. Mutat Res 375:167–81

    CAS  Google Scholar 

  • Fan JL, Wei XG, Wan LC, Zhang LY, Zhao XQ, Liu WZ, Hao HQ, Zhang HY (2011) 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 168:1157–1167

    CAS  Google Scholar 

  • Fidalgo F, Freitas R, Ferreira R, Pessoa AM, Teixeira J (2011) Solanum nigrum L. antioxidant defence system isozymes are regulated transcriptionally and postranslationally in Cd-induced stress. Environ Exp Bot 72:312–319

    CAS  Google Scholar 

  • Gallego SM, Pena LB, Barcia RA, Azpilicueta CE, Iannone MF, Rosales EP, Zawoznik MS, Groppa MD, Benavides MP (2012) Unravelling cadmium toxicity and tolerance in plants: insight into regulatory mechanisms. Environ Exp Bot 83:33–46

    CAS  Google Scholar 

  • Gichner T, Patková Z, Kim J (2003) DNA damage measured by the comet assay in eight agronomic plants. Biol Plant 47:185–188

    CAS  Google Scholar 

  • Gratão PL, Monteiro CC, Tezotto T, Carvalho RF, Alves LR, Peters LP, Azevedo RA (2015) Cadmium stress antioxidant responses and root-to-shoot communication in grafted tomato plants. Biometals 28:803–816

    Google Scholar 

  • Gratão PL, Polle A, Lea PJ, Azevedo RA (2005) Making the life of heavy metal stressed plants a little easier. Funct Plant Biol 32:481–494

    Google Scholar 

  • Gzyl J, Chmielowska-Bak J, Przymusinski R, Gwóźdź EA (2015) Cadmium affects microtubule organization and post-translational modifications of tubulin in seedlings of soybean (Glycine max L.). Front Plant Sci 6:937

    Google Scholar 

  • Hamada T (2007) Microtubule-associated proteins in higher plants. J Plant Res 120:79–98

    CAS  Google Scholar 

  • Hendrix S, Keunen E, Mertens AIG, Beemster GTS, Vangronsveld J, Cuypers A (2018) Cell cycle regulation in different leaves of Arabidopsis thaliana plants grown under control and cadmium-exposed conditions. Environ Exp Bot 155:441–452

    CAS  Google Scholar 

  • Horio T, Murata T (2014) The role of dynamic instability in microtubule organization. Front Plant Sci 5:511

    Google Scholar 

  • Hossain Z, Huq F (2002) Studies on the interaction between Cd2+ ions and DNA. J Inorg Biochem 90:85–96

    CAS  Google Scholar 

  • Iakimova ET, Woltering EJ, Kapchina-Toteva VM, Harren FJM, Cristescu SM (2008) Cadmium toxicity in cultured tomato cells—role of ethylene, proteases and oxidative stress in cell death signaling. Cell Biol Int 32:1521–1529

    CAS  Google Scholar 

  • Kato FH, Carvalho MEA, Gaziola SA, Piotto FA, Azevedo RA (2020) Lysine metabolism and amino acid profile in maize grains from plants subjected to cadmium exposure. Sci Agric 77:e20180095

    Google Scholar 

  • Leme DM, Marin-Morales MA (2009) Allium cepa test in environmental monitoring: a review on its application. Mutat Res 682:71–81

    CAS  Google Scholar 

  • Liu D, Xue P, Meng Q, Zou J, Gu J, Jiang W (2009) Pb/Cu effects on the organization of microtubule cytoskeleton in interphase and mitotic cells of Allium sativum L. Plant Cell Rep 28:695–702

    CAS  Google Scholar 

  • Marques DN, Carvalho MEA, Piotto FA, Batagin-Piotto KD, Nogueira ML, Gaziola SA, Azevedo RA (2019) Antioxidant defense response in plants to cadmium stress. In: Hasanuzzaman M, Prasad MNV, Nahar M (eds) Cadmium tolerance in plants: agronomic, molecular, signaling, and omic approaches, 1st edn. Academic Press, Cambridge, p 423–461

    Google Scholar 

  • Marschner P (2012) Marschner’s mineral nutrition of higher plants. Academic Press, San Diego

    Google Scholar 

  • Michaeli S, Galili G (2014) Degradation of organelles or specific organelle components via selective autophagy in plant cells. Int J Mol Sci 15:7624–7638

    Google Scholar 

  • Mondin M, Santos-Serejo JA, Aguiar-Perecin MLR (2007) Karyotype characterization of Crotalaria juncea (L.) by chromosome banding and physical mapping of 18S-5.8S-26S and 5S rRNA gene sites. Genet Mol Biol 30:65–72

    CAS  Google Scholar 

  • Nogueirol RC, Monteiro FA, Gratão PL, Silva BKA, Azevedo RA (2016) Cadmium application in tomato: nutritional imbalance and oxidative stress. Water Air Soil Pollut 227:210

    Google Scholar 

  • Nogueirol RC, Monteiro FA, Souza Jr JC, Azevedo RA (2018) NO3 −/NH4 + proportions affect cadmium bioaccumulation and tolerance of tomato. Environ Sci Pollut Res 25:13916–13928

    CAS  Google Scholar 

  • O’Lexy R, Kasai K, Clark N, Fujiwara T, Sozzani R, Gallaghe KL (2018) Exposure to heavy metal stress triggers changes in plasmodesmatal permeability via deposition and breakdown of callose. J Exp Bot 69:3715–3728

    Google Scholar 

  • Oldenburg DJ, Bendich AJ (2015) DNA maintenance in plastids and mitochondria of plants. Front Plant Sci 6:883

    Google Scholar 

  • Parrotta L, Cresti M, Cai G (2014) Accumulation and post-translational modifications of plant tubulins. Plant Biol 16:521–527

    CAS  Google Scholar 

  • Piotto FA, Carvalho MEA, Souza LA, Rabêlo FHS, Franco MR, Batagin-Piotto KB, Azevedo RA (2018) Estimating tomato tolerance to heavy metal toxicity: cadmium as study case. Environ Sci Pollut Res 25:27535–27544

    CAS  Google Scholar 

  • Pompeu GB, Vilhena MB, Gratão PL, Carvalho RF, Rossi ML, Martinelli AP, Azevedo RA (2017) Abscisic acid-deficient sit tomato mutant responses to cadmium-induced stress. Protoplasma 254:771–783

    CAS  Google Scholar 

  • R Development Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

  • Sebastian A, Prasad MNV (2016) Modulatory role of mineral nutrients on cadmium accumulation and stress tolerance in Oryza sativa L. seedlings. Environ Sci Pollut Res 23:1224–1233

    CAS  Google Scholar 

  • Seth CS, Misraa V, Chauhan LKS, Singh RR (2008) Genotoxicity of cadmium on root meristem cells of Allium cepa: cytogenetic and comet assay approach. Ecotoxicol Environ Safe 71:711–716

    CAS  Google Scholar 

  • Shi HP, Feng Y, Wang YL, Tsang PKE (2014) Effect of cadmium on cytogenetic toxicity in hairy roots of Wedelia trilobata L. and their alleviation by exogenous CaCl2. Environ Sci Pollut Res 21:1436–1443

    CAS  Google Scholar 

  • Shi Q, Wang J, Zou J, Jiang Z, Wu H, Wang J, Jiang W, Liu D (2016) Cadmium localization and its toxic effects on root tips of barley. Zemdirbyste-Agricultue 103:151–158

    Google Scholar 

  • Siegel S, Castellan NJ (1988) Non parametric statistics for the behavioural sciences. MacGraw Hill Int., New York, NY, p 213–214

    Google Scholar 

  • Singh S, Parihar P, Singh R, Singh VP, Prasad SM (2016) Heavy metal tolerance in plants: role of transcriptomics, proteomics, metabolomics, and ionomics. Front Plant Sci 6:1143

    Google Scholar 

  • Soares C, Carvalho MEA, Azevedo RA, Fidalgo F (2019) Plants facing oxidative challenges—a little help from the antioxidant networks. Environ Exp Bot 161:4–25

    CAS  Google Scholar 

  • Souza LA, Camargos LS, Carvalho MEA (2018) Toxic metal phytoremediation using high biomass non-hyperaccumulator crops: new possibilities for bioenergy resources. In: Matichenkov V (ed) Phytoremediation: methods, management, assessment. Nova Science, New York, NY, p 1–25

    Google Scholar 

  • Wang QL, Liu DH, Yue JY (2016) The uptake of cadmium by Allium cepa var. agrogarum L. and its effects on chromosome and nucleolar behavior in root tip cells. Phyton 85:155–161

    Google Scholar 

  • Wang Y, Ji Y, Fu Y, Guo H (2018) Ethylene-induced microtubule reorientation is essential for fast inhibition of root elongation in Arabidopsis. J Integr Plant Biol 60:864–877

    CAS  Google Scholar 

  • Yakimova ET, Kapchina-Toteva VM, Laarhoven L-J, Harren FM, Woltering EJ (2006) Involvement of ethylene and lipid signalling in cadmium-induced programmed cell death in tomato suspension cells. Plant Physiol Biochem 44:581–589

    CAS  Google Scholar 

  • Zhang S, Zhang H, Qin R, Jiang W, Liu D (2009) Cadmium induction of lipid peroxidation and effects on root tip cells and antioxidant enzyme activities in Vicia faba L. Ecotoxicology 18:814–823

    CAS  Google Scholar 

  • Zhou J, Yao J, Joshi HC (2012) Attachment and tension in the spindle assembly checkpoint. J Cell Sci 115:3547–3555

    Google Scholar 

Download references

Acknowledgements

This work was funded in part by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP—Grant number 2009/54676-0 and scholarship number 2013/15217-5) and the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001. We also thank the National Council for Scientific and Technological Development—CNPq, Brazil and FAPESP, Brazil, for the fellowship and scholarships, respectively.

Author contributions

DP and FAP designed the experiment. DP and MLN carried out the experiments. MFR performed the statistical analysis of the data. DP, FAP, MLN, MM, MEAC and RAA interpreted the results and wrote the manuscript. FAP and RAA assisted during the research. All authors (except MFR, in memorium) read and approved the final manuscript.

Author information

Author notes

  1. These authors contributed equally: Daniel Pizzaia, Marina Lima Nogueira

Authors and Affiliations

  1. Departamento de Genética, Escola Superior de Agricultura “Luiz de Queiroz”, Universidade de São Paulo, Av. Pádua Dias, 11, Piracicaba, SP, 13418-900, Brazil

    Daniel Pizzaia, Marina Lima Nogueira, Mateus Mondin, Marcia Eugenia Amaral Carvalho & Ricardo Antunes Azevedo

  2. Departamento de Produção Vegetal, Escola Superior de Agricultura “Luiz de Queiroz”, Universidade de São Paulo, Av. Pádua Dias, 11, Piracicaba, SP, 13418-900, Brazil

    Fernando Angelo Piotto

  3. Universidade Federal de São Carlos, Campus Lagoa do Sino, Rodovia Lauri Simões de Barros, km 12, SP 189, Buri, SP, 18290-000, Brazil

    Millor Fernandes Rosario

Authors
  1. Daniel Pizzaia
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marina Lima Nogueira
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mateus Mondin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marcia Eugenia Amaral Carvalho
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fernando Angelo Piotto
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Millor Fernandes Rosario
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ricardo Antunes Azevedo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ricardo Antunes Azevedo.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

In memoriam: Millor Fernandes Rosario

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pizzaia, D., Nogueira, M.L., Mondin, M. et al. Cadmium toxicity and its relationship with disturbances in the cytoskeleton, cell cycle and chromosome stability. Ecotoxicology 28, 1046–1055 (2019). https://doi.org/10.1007/s10646-019-02096-0

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-019-02096-0

Keywords

Search

Navigation