Skip to main content
Log in

Cadmium toxicity degree on tomato development is associated with disbalances in B and Mn status at early stages of plant exposure

  • Technical note
  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Cadmium (Cd) toxicity is frequently coupled to its accumulation in plants, but not always the highest Cd concentration triggers the worst damages, indicating that additional events influence the magnitude of Cd side-effects. We investigated the early mechanisms behind the differential Cd-induced impacts on plant development of four tomato accessions with contrasting tolerance to Cd toxicity. At organ level, the highest Cd concentration was not associated with the largest biomass losses. In leaves, changes in superoxide dismutase and catalase activities were not related to differences in Cd concentration, which was unable to provoke H2O2 overproduction on the sixth day of plant exposure to this metal. Further investigation in the mineral profile revealed that magnitude of Cd toxicity depends probably on synergic effects from increased B status, in addition to the own Cd accumulation. Furthermore, disbalances in Mn status (i.e., excess in leaves and deficiency in roots) may enhance Cd toxicity degree. According to data, however, the low magnesium (Mg) status can be linked to tomato tolerance against Cd toxicity. In conclusion, the tomato tolerance degree under short-Cd exposure depends on actively, finely regulation of mineral homeostasis that results in different development of plant organs. The better understanding on the mode of action of Cd toxicity in plants can help in the establishment of strategies to mitigate its impacts on crop yield.

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

References

  • Alexieva V, Sergiev I, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant Cell Environ 24:1337–1344

    Article  CAS  Google Scholar 

  • Alvarenga MAR (2013) Tomate: Produção em campo, em casa-de-vegetação e em hidroponia. Editora Universitária, Lavras (In Portuguese)

    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

    Article  CAS  Google Scholar 

  • Amaral dos Reis R, Keunen E, Mourato MP, Martins LL, Vangronsveld J, Cuypers A (2018) Accession-specific life strategies affect responses in leaves of Arabidopsis thaliana plants exposed to excess Cu and Cd. J Plant Physiol 223:37–46

    Article  CAS  Google Scholar 

  • Azevedo RA, Alas RM, Smith RJ, Lea PJ (1998) Response of antioxidant enzymes to transfer from elevated carbon dioxide to air and ozone fumigation, in the leaves and roots of wild-type and a catalase-deficient mutant of barley. Physiol Plant 104:280–292

    Article  CAS  Google Scholar 

  • Bahmani R, Kim DG, Kim JA, Hwang S (2016) The density and length of root hairs are enhanced in response to cadmium and arsenic by modulating gene expressions involved in fate determination and morphogenesis of root hairs in Arabidopsis. Front Plant Sci 7:1763

    Article  Google Scholar 

  • Baszyńki T, Wajda L, Król M, Wolińska D, Krupa Z, Tukendorf A (1980) Photosynthetic activities of cadmium‐treated tomato plants. Physiol Plant 48:365–370

    Article  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

    Article  CAS  Google Scholar 

  • Borišev M, Pajević S, Nikolić N, Orlović S, Župunski M, Pilipović A, Kebert M (2017) Magnesium and iron deficiencies alter Cd accumulation in Salix viminalis L. J Phytorem 18:164–170

    Article  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein dye-binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Branco-Neves S, Soares C, Sousa A, Martins V, Azenha M, Gerós H, Fidalgo F (2017) An efficient antioxidant system and heavy metal exclusion from leaves make Solanum cheesmaniae more tolerant to Cu than its cultivated counterpart. Food Energy Secur 6:123–133

    Article  Google Scholar 

  • Carvalho FP (2017) Mining industry and sustainable development: time for change. Food Energy Secur 6:61–77

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Cembrowska-Lech D, Koprowski M, Kepczynki J (2015) Germination induction of dormant Avena fatua caryopses by KAR1 and GA3 involving the control of reactive oxygen species (H2O2 and O2−) and enzymatic antioxidants (superoxide dismutase and catalase) both in the embryo and the aleurone layers. J Plant Physiol 176:169–179

    Article  CAS  Google Scholar 

  • Chen H, Zhang C, Guo H, Hu Y, He Y, Jiang D (2018) Overexpression of a Miscanthus sacchariflorus yellow stripe-like transporter MsYSL1 enhances resistance of Arabidopsis to cadmium by mediating metal ion reallocation. Plant Growth Regul 85:101–111

    Article  CAS  Google Scholar 

  • Chou T-S, Chao Y-Y, Huang W-D, Hong C-Y, Kao C-H (2011) Effect of magnesium deficiency on antioxidant status and cadmium toxicity in rice seedlings. J Plant Physiol 168:1021–1030

    Article  CAS  Google Scholar 

  • Cuypers AC, Hendrix S, Reis RA, Smet S, Deckers J, Gielen H, Jozefczak M, Loix C, Vercampt H, Vangronsveld J, Keunen E (2016) Hydrogen peroxide, signaling in disguise during metal phytotoxicity. Front Plant Sci 7:470

    Article  Google Scholar 

  • Delpérée C, Lutts S (2008) Growth inhibition occurs independently of cell mortality in tomato (Solanum lycopersicum) exposed to high cadmium concentrations. J Integr Plant Biol 50:300–310

    Article  Google Scholar 

  • Djebali W, Hédiji H, Abbes Z, Barhoumi Z, Yaakoubi H, Zoghlami LB, Chábi W (2010) Aspects on growth and anatomy of internodes and leaves of cadmium-treated Solanum lycopersicum L. plants. J Biol Res 13:75–84

    CAS  Google Scholar 

  • Durenne B, Druart P, Blondel A, Fauconnier M-L (2018) How cadmium affects the fitness and the glucosinolate content of oilseed rape plantlets. Environ Exp Bot 155:185–194

    Article  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 posttranslationally in Cd-induced stress. Environ Exp Bot 72:312–319

    Article  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

    Article  CAS  Google Scholar 

  • Gratão PL, Monteiro CC, Rossi ML, Martinelli AP, Peres LEP, Medici LO, Lea PJ, Azevedo RA (2009) Differential ultrastructural changes in tomato hormonal mutants exposed to cadmium. Environ Exp Bot 67:387–394

    Article  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

    Article  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

    Article  Google Scholar 

  • Hasan MK, Liu C, Wang F, Ahammed GJ, Zhou J, Xu M-X, Yu J-Q, Xia XJ (2016) Glutathione-mediated regulation of nitric oxide, S-nitrosothiol and redox homeostasis confers cadmium tolerance by inducing transcription factors and stress response genes in tomato. Chemosphere 161:536–545

    Article  CAS  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    Article  CAS  Google Scholar 

  • Hédiji H, Djebali W, Belkadhi A, Cabasson C, Moing A, Rolin D, Brouquisse R, Gallusci P, Chaïbi W (2015) Impact of long-term cadmium exposure on mineral content of Solanum lycopersicum plants: consequences on fruit production. S Afr J Bot 97:176–181

    Article  Google Scholar 

  • Hermans C, Chen J, Coppens F, Inzé D, Verbruggen N (2011) Low magnesium status in plants enhances tolerance to cadmium exposure. New Phytol 192:428–436

    Article  CAS  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Dissertation, University of California

  • Hussain MM, Saeed A, Khan AA, Javid S, Fatima B (2015) Differential responses of one hundred tomato cultivars grown under cadmium stress. Genet Mol Res 14:13162–13171

    Article  CAS  Google Scholar 

  • Iannone MF, Groppa MD, Benavides MP (2015) Cadmium induces different biochemical responses in wild type and catalase-deficient-tobacco plants. Environ Exp Bot 109:201–211

    Article  CAS  Google Scholar 

  • Jia L, Liu Z, Chen W, Ye Y, Yu S, He X (2015) Hormesis effects induced by cadmium on growth and photosynthetic performance in a hyperaccumulator, Lonicera japonica Thunb. J Plant Growth Regul 34:13

    Article  CAS  Google Scholar 

  • Kabata-Pendias A (2011) Cadmium. In: Kabata-Pendias A (ed) Trace elements in soils and plants. CRC Press, Boca Raton, p 287–304

    Google Scholar 

  • Kanai S, Ohkura K, Adu-Gyamfi J, Mohapatra PK, Nguyen NT, Saneoka H, Fujita K (2007) Depression of sink activity precedes the inhibition of biomass production in tomato plants subjected to potassium deficiency stress. J Exp Bot 58:2917–2928

    Article  CAS  Google Scholar 

  • Kar M (2018) Determination of the expression level of stress-related genes in Cicer arietinum root cell under Cd stress and the relationship to H2O2 concentrations. Ecotoxicology [in press]. https://doi.org/10.1007/s10646-018-1961-1

    Article  CAS  Google Scholar 

  • Kaya C, Tuna AL, Dikilitas M, Ashraf M, Koskeroglu S, Guneri M (2009) Supplementary phosphorus can alleviate boron toxicity in tomato. Sci Hort 121:284–288

    Article  CAS  Google Scholar 

  • Kono Y, Fridovich I (1982) Superoxide radical inhibits catalase. J Biol Chem 257:5751–5754

    CAS  Google Scholar 

  • Kudo H, Kudo K, Uemura M, Kawai S (2015) Magnesium inhibits cadmium translocation from roots to shoots, rather than the uptake from roots, in barley. Botany 93:345–351

    Article  CAS  Google Scholar 

  • Kumar P, Edelstein M, Cardarelli M, Ferri E, Colla G (2015) Grafting affects growth, yield, nutrient uptake, and partitioning under cadmium stress in tomato. HortScience 50:1654–1661

    CAS  Google Scholar 

  • Kuznetsov ML, Teixeira FA, Bokach NA, Pombeiro AJL, Shul’pin GB (2014) Radical decomposition of hydrogen peroxide catalyzed by aqua complexes [M(H2O)n]2+(M=Be, Zn, Cd). J Catal 313:135–148

    Article  CAS  Google Scholar 

  • Lavres Junior L, Reis AR, Rossi ML, Cabral CP, Nogueira NL, Malavolta E (2010) Changes in the ultrastructure of soybean cultivars in response to manganese supply in solution culture. Sci Agric 67:287–294

    Article  Google Scholar 

  • Lidon FC, Teixeira MG (2000) Rice tolerance to excess Mn: Implications in the chloroplast lamellae and synthesis of a novel Mn protein. Plant Physiol Biochem 38:969–978

    Article  CAS  Google Scholar 

  • Liu H, Zhang Y, Chai T, Tan J, Wang J, Feng S, Liu G (2013) Manganese-mitigation of cadmium toxicity to seedling growth of Phytolacca acinosa Roxb. is controlled by the manganese/cadmium molar ratio under hydroponic conditions. Plant Physiol Biochem 73:144–153

    Article  CAS  Google Scholar 

  • Loix C, Huybrechts M, Vangronsveld J, Gielen M, Keunen E, Cuypers A (2017) Reciprocal Interactions between cadmium-induced cell wall responses and oxidative stress in plants. Front Plant Sci 8:1867

    Article  Google Scholar 

  • Migocka M, Klobus G (2007) The properties of the Mn, Ni and Pb transport operating at plasma membranes of cucumber roots. Physiol Plant 129:578–587

    Article  CAS  Google Scholar 

  • Perfus-Barbeoch L, Leonhardt N, Vavasseur A, Forestier C (2002) Heavy metal toxicity: cadmium permeates through calcium channels and disturbs the plant water status. Plant J 32:539–548

    Article  CAS  Google Scholar 

  • Piotto FA (2012) Evaluation of cadmium tolerance in tomato (Solanum lycopersicum L.). Thesis. Escola Superior de Agricultura Luiz de Queiroz/ Universidade de São Paulo

  • 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

    Article  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

    Article  CAS  Google Scholar 

  • Rahman A, Nahar K, Hasanuzzaman M, Fujita M (2016) Manganese-induced cadmium stress tolerance in rice seedlings: Coordinated action of antioxidant defense, glyoxalase system and nutrient homeostasis. Comptes Rendus Biol 339:462–474

    Article  Google Scholar 

  • Ramos I, Esteban E, Lucena JJ, Gárate A (2002) Cadmium uptake and subcellular distribution in plants of Lactuca sp. Cd–Mn interaction. Plant Sci 162:761–767

    Article  CAS  Google Scholar 

  • Reid R, Fitzpatrick K (2009) Influence of leaf tolerance mechanisms and rain on boron toxicity in barley and wheat. Plant Physiol 151:413–420

    Article  CAS  Google Scholar 

  • Santos EF, Santini JMK, Paixao AP, Furlani Júnior E, Lavres J, Campos M, Reis AR (2017) Physiological highlights of manganese toxicity symptoms in soybean plants: Mn toxicity responses. Plant Physiol Biochem 113:6–19

    Article  CAS  Google Scholar 

  • SAS Institute (2011) SAS/STAT User’s Guide: Version 9.3. SAS Institute, Cary

    Google Scholar 

  • Sasaki A, Yamaji N, Yokosho K, Ma JF (2012) Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell 24:2155–2167

    Article  CAS  Google Scholar 

  • 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

    Article  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. Zemdirb Agric 103(2):151–158

    Article  Google Scholar 

  • Siddiqui MH, Al-Whaibi MH, Sakran AM, Basalah MO, Ali HM (2012) Effect of calcium and potassium on antioxidant system of Vicia faba L. under cadmium stress. Int J Mol Sci 13:6604–6619

    Article  CAS  Google Scholar 

  • Song J, Feng SJ, Chen J, Zhao WT, Yang ZM (2017) A cadmium stress-responsive gene AtFC1 confers plant tolerance to cadmium toxicity. BMC Plant Biol 17:187

    Article  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 

  • Souza LA, Monteiro CC, Carvalho RF, Gratão PL, Azevedo RA (2017) Dealing with abiotic stresses: An integrative view of how phytohormones control abiotic stress-induced oxidative stress. Theor Exp Plant Physiol 29:109–127

    Article  CAS  Google Scholar 

  • Štolfa I, Pfeiffer TŽ, Špoljarić D, Teklić T, Lončarić Z (2015) Heavy metal-induced oxidative stress in plants: response of the antioxidative system. In: Gupta D, Palma J, Corpas F (eds) Reactive oxygen species and oxidative damage in plants under stress. Springer Inter Pub, Switzerland, p 127–163

    Chapter  Google Scholar 

  • Teklić T, Lončarić Z, Kovačević V, Singh BR (2013) Metallic trace elements in cereal grain—a review: How much metal do we eat? Food Energy Secur 2:81–95

    Article  Google Scholar 

  • Tkalec M, Štefanić PP, Cvjetko P, Šikić S, Pavlica M, Balen B (2014) The effects of cadmium–zinc interactions on biochemical responses in tobacco seedlings and adult plants. Plos One 9:e87582

    Article  Google Scholar 

  • Uraguchi S, Kiyono M, Sakamoto T, Watanabe I, Kuno K (2009) Contributions of apoplasmic cadmium accumulation, antioxidative enzymes and induction of phytochelatins in cadmium tolerance of the cadmium-accumulating cultivar of black oat (Avena strigosa Schreb.). Planta 230:267–276

    Article  CAS  Google Scholar 

  • Wang X, Shi M, Hao P, Zheng W, Cao F (2017) Alleviation of cadmium toxicity by potassium supplementation involves various physiological and biochemical features in Nicotiana tabacum L. Acta Physiol Plant 39:132

    Article  Google Scholar 

  • Weber M, Trampczynska A, Clemens S (2006) Comparative transcriptome analysis of toxic metal responses in Arabidopsis thaliana and the Cd2+-hypertolerant facultative metallophyte Arabidopsis halleri. Plant Cell Environ 29:950–963

    Article  CAS  Google Scholar 

  • Wu D, Yamaji N, Yamane M, Kashino-Fujii M, Sato K, Ma JF (2016) The HvNramp5 transporter mediates uptake of cadmium and manganese, but not iron. Plant Physiol 172:1899–1910

    Article  CAS  Google Scholar 

  • Wu J, Guo J, Hu Y, Gong H (2015) Distinct physiological responses of tomato and cucumber plants in silicon-mediated alleviation of cadmium stress. Front Plant Sci 6:453

    Google Scholar 

  • Zheng J, Gu XQ, Zhang TJ, Liu HH, Ou QJ, Peng CL (2018) Phytotoxic effects of Cu, Cd and Zn on the seagrass Thalassia hemprichii and metal accumulation in plants growing in Xincun Bay, Hainan, China. Ecotoxicology [in press], https://doi.org/10.1007/s10646-018-1924-6

    Article  CAS  Google Scholar 

  • Zornoza P, Sánchez-Pardo B, Carpena RO (2010) Interaction and accumulation of manganese and cadmium in the manganese accumulator Lupinus albus. J Plant Physiol 167:1027–1032

    Article  CAS  Google Scholar 

Download references

Funding

This work was funded by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP—Grant number 2009/54676-0 to R.A.A.). We thank Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (R.A.A., M.R.F, and K.L.R), and FAPESP (M.E.A.C.) for the fellowship and scholarships granted (2013/15217-5).

Author contributions

M.E.A.C. and F.A.P. designed the experiment. M.E.A.C. carried out the experiments with the help of M.R.F., K.L.R. and S.A.G. M.E.A.C. analyzed the data, interpreted the results and wrote the manuscript. P.R.C.C. and R.A.A. assisted during the research and writing the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ricardo Antunes Azevedo.

Ethics declarations

Conflict of interests

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Carvalho, M.E.A., Piotto, F.A., Franco, M.R. et al. 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 (2018). https://doi.org/10.1007/s10646-018-1983-8

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-018-1983-8

Keywords

Navigation