, Volume 27, Issue 10, pp 1293–1302 | Cite as

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

  • Marcia Eugenia Amaral Carvalho
  • Fernando Angelo Piotto
  • Mônica Regina Franco
  • Karina Lima Reis Borges
  • Salete Aparecida Gaziola
  • Paulo Roberto Camargo Castro
  • Ricardo Antunes AzevedoEmail author
Technical note


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.


Boron phytotoxicity Heavy metal Magnesium status Manganese toxicity Solanum lycopersicum Tolerance level 



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.

Compliance with ethical standards

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.


  1. 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 24:1337–1344CrossRefGoogle Scholar
  2. Alvarenga MAR (2013) Tomate: Produção em campo, em casa-de-vegetação e em hidroponia. Editora Universitária, Lavras (In Portuguese)Google Scholar
  3. 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 134:102–115CrossRefGoogle Scholar
  4. 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 223:37–46CrossRefGoogle Scholar
  5. 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 104:280–292CrossRefGoogle Scholar
  6. 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 7:1763CrossRefGoogle Scholar
  7. Baszyńki T, Wajda L, Król M, Wolińska D, Krupa Z, Tukendorf A (1980) Photosynthetic activities of cadmium‐treated tomato plants. Physiol Plant 48:365–370CrossRefGoogle Scholar
  8. 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 27:245–258CrossRefGoogle Scholar
  9. 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 18:164–170CrossRefGoogle Scholar
  10. Bradford MM (1976) A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein dye-binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  11. 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 6:123–133CrossRefGoogle Scholar
  12. Carvalho FP (2017) Mining industry and sustainable development: time for change. Food Energy Secur 6:61–77CrossRefGoogle Scholar
  13. 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:e00131CrossRefGoogle Scholar
  14. 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 255:989–999CrossRefGoogle Scholar
  15. 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 176:169–179CrossRefGoogle Scholar
  16. 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 85:101–111CrossRefGoogle Scholar
  17. 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 168:1021–1030CrossRefGoogle Scholar
  18. 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 7:470CrossRefGoogle Scholar
  19. 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 50:300–310CrossRefGoogle Scholar
  20. 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 13:75–84Google Scholar
  21. 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 155:185–194CrossRefGoogle Scholar
  22. 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 72:312–319CrossRefGoogle Scholar
  23. 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 83:33–46CrossRefGoogle Scholar
  24. 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 67:387–394CrossRefGoogle Scholar
  25. 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 28:803–816CrossRefGoogle Scholar
  26. Gratão PL, Polle A, Lea PJ, Azevedo RA (2005) Making the life of heavy metal stressed plants a little easier. Funct Plant Biol 32:481–494CrossRefGoogle Scholar
  27. 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 161:536–545CrossRefGoogle Scholar
  28. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198CrossRefGoogle Scholar
  29. 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 97:176–181CrossRefGoogle Scholar
  30. Hermans C, Chen J, Coppens F, Inzé D, Verbruggen N (2011) Low magnesium status in plants enhances tolerance to cadmium exposure. New Phytol 192:428–436CrossRefGoogle Scholar
  31. Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Dissertation, University of CaliforniaGoogle Scholar
  32. 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 14:13162–13171CrossRefGoogle Scholar
  33. Iannone MF, Groppa MD, Benavides MP (2015) Cadmium induces different biochemical responses in wild type and catalase-deficient-tobacco plants. Environ Exp Bot 109:201–211CrossRefGoogle Scholar
  34. 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 34:13CrossRefGoogle Scholar
  35. Kabata-Pendias A (2011) Cadmium. In: Kabata-Pendias A (ed) Trace elements in soils and plants. CRC Press, Boca Raton, p 287–304Google Scholar
  36. 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 58:2917–2928CrossRefGoogle Scholar
  37. 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]. CrossRefGoogle Scholar
  38. Kaya C, Tuna AL, Dikilitas M, Ashraf M, Koskeroglu S, Guneri M (2009) Supplementary phosphorus can alleviate boron toxicity in tomato. Sci Hort 121:284–288CrossRefGoogle Scholar
  39. Kono Y, Fridovich I (1982) Superoxide radical inhibits catalase. J Biol Chem 257:5751–5754Google Scholar
  40. 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 93:345–351CrossRefGoogle Scholar
  41. 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 50:1654–1661Google Scholar
  42. 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 313:135–148CrossRefGoogle Scholar
  43. 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 67:287–294CrossRefGoogle Scholar
  44. 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 38:969–978CrossRefGoogle Scholar
  45. 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 73:144–153CrossRefGoogle Scholar
  46. 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 8:1867CrossRefGoogle Scholar
  47. Migocka M, Klobus G (2007) The properties of the Mn, Ni and Pb transport operating at plasma membranes of cucumber roots. Physiol Plant 129:578–587CrossRefGoogle Scholar
  48. 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 32:539–548CrossRefGoogle Scholar
  49. Piotto FA (2012) Evaluation of cadmium tolerance in tomato (Solanum lycopersicum L.). Thesis. Escola Superior de Agricultura Luiz de Queiroz/ Universidade de São PauloGoogle Scholar
  50. 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 25:27535–27544CrossRefGoogle Scholar
  51. 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 254:771–783CrossRefGoogle Scholar
  52. 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 339:462–474CrossRefGoogle Scholar
  53. Ramos I, Esteban E, Lucena JJ, Gárate A (2002) Cadmium uptake and subcellular distribution in plants of Lactuca sp. Cd–Mn interaction. Plant Sci 162:761–767CrossRefGoogle Scholar
  54. Reid R, Fitzpatrick K (2009) Influence of leaf tolerance mechanisms and rain on boron toxicity in barley and wheat. Plant Physiol 151:413–420CrossRefGoogle Scholar
  55. 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 113:6–19CrossRefGoogle Scholar
  56. SAS Institute (2011) SAS/STAT User’s Guide: Version 9.3. SAS Institute, CaryGoogle Scholar
  57. Sasaki A, Yamaji N, Yokosho K, Ma JF (2012) Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell 24:2155–2167CrossRefGoogle Scholar
  58. 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 23:1224–1233CrossRefGoogle Scholar
  59. 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):151–158CrossRefGoogle Scholar
  60. 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 13:6604–6619CrossRefGoogle Scholar
  61. 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 17:187CrossRefGoogle Scholar
  62. 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 1–25Google Scholar
  63. 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 29:109–127CrossRefGoogle Scholar
  64. 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 127–163CrossRefGoogle Scholar
  65. 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 2:81–95CrossRefGoogle Scholar
  66. 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:e87582CrossRefGoogle Scholar
  67. 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 230:267–276CrossRefGoogle Scholar
  68. 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 39:132CrossRefGoogle Scholar
  69. 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 29:950–963CrossRefGoogle Scholar
  70. 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 172:1899–1910CrossRefGoogle Scholar
  71. 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 6:453Google Scholar
  72. 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], CrossRefGoogle Scholar
  73. Zornoza P, Sánchez-Pardo B, Carpena RO (2010) Interaction and accumulation of manganese and cadmium in the manganese accumulator Lupinus albus. J Plant Physiol 167:1027–1032CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Marcia Eugenia Amaral Carvalho
    • 1
  • Fernando Angelo Piotto
    • 2
  • Mônica Regina Franco
    • 1
  • Karina Lima Reis Borges
    • 1
  • Salete Aparecida Gaziola
    • 1
  • Paulo Roberto Camargo Castro
    • 3
  • Ricardo Antunes Azevedo
    • 1
    Email author
  1. 1.Departamento de Genética, Escola Superior de Agricultura “Luiz de Queiroz”Universidade de São Paulo (Esalq/USP)PiracicabaBrazil
  2. 2.Departamento de Produção Vegetal, Escola Superior de Agricultura “Luiz de Queiroz”Universidade de São Paulo (Esalq/ USP)PiracicabaBrazil
  3. 3.Departamento de Ciências Biológicas, Escola Superior de Agricultura “Luiz de Queiroz”Universidade de São Paulo (Esalq/ USP)PiracicabaBrazil

Personalised recommendations