Biologia Plantarum

, Volume 62, Issue 3, pp 543–550 | Cite as

The crucial role of roots in increased cadmium-tolerance and Cd-accumulation in the pea mutant SGECdt

  • A. A. Belimov
  • N. V. Malkov
  • J. V. Puhalsky
  • V. E. Tsyganov
  • K. B. Bodyagina
  • V. I. Safronova
  • K.-J. Dietz
  • I. A. Tikhonovich
Original paper


Elucidation of mechanisms underlying plant tolerance to cadmium, a widespread toxic soil pollutant, and accumulation of Cd in plants are urgent tasks. For this purposes, the pea (Pisum sativum L.) mutant SGECdt (obtained by treatment of the laboratory pea line SGE with ethylmethane sulfonate) was reciprocally grafted with the parental line SGE, and four scion/rootstock combinations were obtained: SGE/SGE, SGECdt/SGECdt, SGE/SGECdt, and SGECdt/SGE. They were grown in hydroponics in the presence of 1 μM CdCl2 for 30 d. The SGE and SGECdt scions on the SGECdt rootstock had a higher root and shoot biomass and an elevated root and shoot Cd content compared with the grafts having SGE rootstock. Only the grafts with the SGE rootstock showed chlorosis and roots demonstrating symptoms of Cd toxicity. The content of nutrient elements in roots (Fe, K, Mg, Mn, Na, P, and Zn) was higher in the grafts having the SGECdt rootstock, and three elements, namely Ca, Fe, and Mn, were efficiently transported by the SGECdt root to the shoot of these grafts. The content of other measured elements (K, Mg, Na, P, and Zn) was similar in the root and shoot in all the grafts. Then, the non-grafted plants were grown in the presence of Cd and subjected to deficit or excess concentrations of Ca, Fe, or Mn. Exclusion of these elements from the nutrient solution retained or increased differences between SGE and SGECdt in growth response to Cd toxicity, whereas excess of Ca, Fe, or Mn decreased or eliminated such differences. The obtained results assign a principal role of roots to realizing the increased Cd-tolerance and Cdaccumulation in the SGECdt mutant. Efficient translocation of Ca, Fe, and Mn from roots to shoots appeared to counteract Cd toxicity, although Cd was actively taken up by roots and accumulated in shoots.

Additional key words

calcium grafting heavy metals iron magnesium manganese phosphorus potassium sodium zinc 





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  1. Belimov, A.A., Dodd, I.C., Safronova, V.I., Malkov, N.V., Davies, W.J., Tikhonovich, I.A.: The cadmium tolerant pea (Pisum sativum L.) mutant SGECd t is more sensitive to mercury: assessing plant water relations. - J. exp. Bot. 66: 2359–2369, 2015.CrossRefPubMedPubMedCentralGoogle Scholar
  2. Belimov, A.A., Malkov, N.V., Puhalsky, J.V., Safronova, V.I., Tikhonovich, I.A.: High specificity in response of pea mutant SGECd t to toxic metals: growth and element composition. - Environ. exp. Bot. 128: 91–98, 2016.CrossRefGoogle Scholar
  3. Cataldo, D.A., Garland, T.R., Wildung, R.E.: Cadmium uptake kinetics in intact soybean plants. - Plant Physiol. 73: 844–848, 1983.CrossRefPubMedPubMedCentralGoogle Scholar
  4. Cho, S.-C., Chao, Y.-Y., Kao, C.H.: Calcium deficiency increases Cd toxicity and Ca is required for heat-shock induced Cd tolerance in rice seedlings. - J. Plant Physiol. 169: 892–898, 2012.CrossRefPubMedGoogle Scholar
  5. Cobbett, C.S., May, M.J., Howden, R., Rolls, B.: The glutathione-deficient, cadmium sensitive mutant, cad2-1, of Arabidopsis thaliana is deficient in γ-glutamylcysteine synthetase. - Plant J. 16: 73–78, 1998.CrossRefPubMedGoogle Scholar
  6. Disante, K.B., Cortina, J., Vilagrosa, A., Fuentes, D., Hernández, E.I., Ljung, K.: Alleviation of Zn toxicity by low water availability. - Physiol. Plant. 150: 412–424, 2014.CrossRefPubMedGoogle Scholar
  7. Dong, J., Mao, W.H., Zhang, G.P., Wu, F.B., Cai, Y.: Root excretion and plant tolerance to cadmium toxicity–a review. - Plant Soil Environ. 53: 193–200, 2007.CrossRefGoogle Scholar
  8. Drazkiewicz, M., Baszynski, T.: Calcium protection of PS2 complex of Phaseolus coccineus from cadmium toxicity: in vitro study. - Environ. exp. Bot. 64: 8–14, 2008.CrossRefGoogle Scholar
  9. Hasan, S.A., Fariduddin, Q., Ali, B., Hayat, S., Ahmad, A.: Cadmium: toxicity and tolerance in plants. - J. environ. Biol. 30: 165–174, 2009.PubMedGoogle Scholar
  10. He, J.Y., Ren, Y.F., Wang, F.J., Pan, X.B., Zhu, C., Jiang, D.A.: Characterization of cadmium uptake and translocation in a cadmium-sensitive mutant of rice (Oryza sativa L. ssp. japonica). - Arch. Environ. Contam. Toxicol. 57: 299–306, 2009.CrossRefPubMedGoogle Scholar
  11. He, Z., Li, J., Zhang, H., Ma, M.: Different effects of calcium and lanthanum on the expression of phytochelatin synthase gene and cadmium absorption in Lactuca sativa. - Plant Sci. 168: 309–318, 2005.CrossRefGoogle Scholar
  12. Howden, R., Goldsbrough, P.B., Andersen, C.R., Cobbett, C.S.: Cadmium-sensitive, cad1 mutants of Arabidopsis thaliana are phytochelatin deficient. - Plant Physiol. 107: 1059–1066, 1995.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Huang, Q.N., An, H., Yang, Y.J., Liang, Y., Shao, G.S.: Effects of Mn-Cd antagonistic interaction on Cd accumulation and major agronomic traits in rice genotypes by different Mn forms. - Plant Growth Regul. 82: 317–331, 2017.CrossRefGoogle Scholar
  14. Kulaeva, O.A., Tsyganov, V.E.: Molecular-genetic basis of cadmium tolerance and accumulation in higher plants. - Russ. J. Genet. appl. Res. 1: 349–360, 2011.CrossRefGoogle Scholar
  15. Kulaeva, O.A., Tsyganov, V.E.: Fine mapping of a cdt locus mutation that leads to an increase in the tolerance of pea (Pisum sativum L.) to cadmium. - Russ. J. Genet. appl. Res. 3: 120–126, 2013.CrossRefGoogle Scholar
  16. Kulaeva, O.A., Tsyganov, V.E.: Gene expression analysis of genes coding key enzymes of cadmium detoxification in garden pea symbiotic nodules. - Russ. J. Genet. appl. Res. 5: 479–485, 2015.CrossRefGoogle Scholar
  17. Larsson, E.H., Asp, H., Bornman, J.F.: Influence of prior Cd2+ exposure on the uptake of Cd2+ and other elements in the phytochelatin-deficient mutant, cad1-3, of Arabidopsis thaliana. - J. exp. Bot. 53: 447–453, 2002.CrossRefPubMedGoogle Scholar
  18. Lefevre, I., Marchal, G., Meerts, P., Correal, E., Lutts, S.: Chloride salinity reduces cadmium accumulation by the Mediterranean halophyte species Atriplex halimus L. - Environ. exp. Bot. 65: 142–152, 2009.CrossRefGoogle Scholar
  19. Lin, Y.F., Aarts, G.M.: The molecular mechanism of zinc and cadmium stress response in plants. - Cell. Mol. Life Sci. 69: 3187–3206, 2012.CrossRefPubMedGoogle Scholar
  20. Liu, H., Zhang, Y., Chai, T., Tan, J., Wang, J., Feng, S., Liu, G.: 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, 2013.CrossRefPubMedGoogle Scholar
  21. Nazar, R., Iqbal, N., Masood, A., Iqbal, M., Khan, R., Syeed, S., Khan, N.A.: Cadmium toxicity in plants and role of mineral nutrients in its alleviation. - Amer. J. Plant Sci. 3: 1476–1489, 2012.CrossRefGoogle Scholar
  22. Nedjimi, B., Daoud, Y.: Cadmium accumulation in Atriplex halimus subsp. schweinfurthii and its influence on growth, proline, root hydraulic conductivity and nutrient uptake. - Flora 204: 316–324, 2009.CrossRefGoogle Scholar
  23. Palove-Balang, P., Kisova, A., Pavlovkin, J., Mistrik, I.: Effect of manganese on cadmium toxicity in maize seedlings. - Plant Soil Environ. 52: 143–149, 2006.CrossRefGoogle Scholar
  24. Peng, K., Chunling, C., You, W., Lian, C., Li, X., Shen, Z.: Manganese uptake and interactions with cadmium in the hyperaccumulator–Phytolacca Americana L. - J. Hazard. Mater. 154: 674–681, 2008.CrossRefPubMedGoogle Scholar
  25. Perfus-Barbeoch, L., Leonhardt, L., Vavasseur, A., Forestier, C.: Heavy metal toxicity: cadmium permeates through calcium channels and disturbs the plant water status. - Plant J. 32: 539–548, 2002.CrossRefPubMedGoogle Scholar
  26. Pittman, J.K.: Managing the manganese: molecular mechanisms of manganese transport and homeostasis. - New Phytol. 167: 733–742, 2005.CrossRefPubMedGoogle Scholar
  27. Pollard, A.J., Reeves, R.D., Baker, A.J.M.: Facultative hyperaccumulation of heavy metals and metalloids. - Plant Sci. 217–218: 8–17, 2014.CrossRefPubMedGoogle Scholar
  28. Poschenrieder, C., Barcelo, J.: Water relations in heavy metal stressed plants. - In: Prasad, M.N.V., Hagemeyer, J. (ed.): Heavy Metal Stress in Plants: from Molecules to Ecosystems. Pp. 207–209. Springer-Verlag, Berlin - Heidelberg 1999.CrossRefGoogle Scholar
  29. Rahman, A., Nahar, K., Hasanuzzaman, M., Fujita, M.: Manganese-induced cadmium stress tolerance in rice seedlings: Coordinated action of antioxidant defense, glyoxalase system and nutrient homeostasis. - Compt. rend. Biol. 339: 462–474, 2016.CrossRefGoogle Scholar
  30. Rodriguez-Hernandez, M.C., Bonifas, I., Alfaro-De la Torre, M.C., Flores-Flores, J.L., Banuelos-Hernandez, B., Patino-Rodriguez, O.: Increased accumulation of cadmium and lead under Ca and Fe deficiency in Typha latifolia: A study of two pore channel (TPC1) gene responses. - Environ. exp. Bot. 115: 38–48, 2015.CrossRefGoogle Scholar
  31. Rodriguez-Serrano, M., Romero-Puertas, M.C., Pazmino, D.M., Testillano, P.S., Risueno, M.C., Del Rio, L.A., Sandalio, L.M.: Cellular response of pea plants to cadmium toxicity: cross talk between reactive oxygen species, nitric oxide, and calcium. - Plant Physiol. 150: 229–243, 2009.CrossRefPubMedPubMedCentralGoogle Scholar
  32. Sanita di Toppi, L., Gabrielli, R.: Response to cadmium in higher plants. - Environ. exp. Bot. 41: 105–130, 1999.CrossRefGoogle Scholar
  33. Sharma, S.S., Dietz, K.J., Mimura, T.: Vacuolar compartmentalization as indispensable component of heavy metal detoxification in plants. - Plant Cell Environ. 39: 1112–1126, 2016.CrossRefPubMedGoogle Scholar
  34. Shen, G.M., Zhu, C., Shangguan, L.-N., Du, Q.-Z.: The Cdtolerant rice mutant cadH-5 is a high Cd accumulator and shows enhanced antioxidant activity. - J. Plant Nutr. Soil Sci. 175: 309–318, 2012.CrossRefGoogle Scholar
  35. Sterckeman, T., Redjala, T., Morel, J.L.: Influence of exposure solution composition and of plant cadmium content on root cadmium short-term uptake. - Environ. exp. Bot. 74: 131–139, 2011.CrossRefGoogle Scholar
  36. Thys, C., Vanthomme, P., Schrevens, E., De Proft, M.: Interactions of Cd with Zn, Cu, Mn and Fe for lettuce (Lactuca sativa L.) in hydroponic culture. - Plant Cell Environ. 14: 713–717, 1991.CrossRefGoogle Scholar
  37. Tsyganov, V.E., Belimov, A.A., Borisov, A.Y., Safronova, V.I., Georgi, M., Dietz, K.J., Tikhonovich, I.A.: A chemically induced new pea (Pisum sativum L.) mutant SGECd t with increased tolerance to and accumulation of cadmium. - Ann. Bot. 99: 227–237, 2007.CrossRefPubMedPubMedCentralGoogle Scholar
  38. Tsyganov, V.E., Kulaeva, O.A., Knox, M.R., Borisov, A.Y., Tikhonovich, I.A., Ellis, T.H.N.: Using of SSAP analysis for primary localization of mutation cdt (Cadmium tolerance) in pea linkage group VI. - Russ. J. Genet. appl. Res. 3: 152–155, 2013.CrossRefGoogle Scholar
  39. Tsyganov, V.E., Zhernakov, A.I., Khodorenko, A.V., Kisutin, P.Y., Belimov, A.A., Safronova, V.I., Naumkina, T.S., Borisov, A.Y., Lindblad, P., Dietz, K.J., Tikhonovich, I.A.: Mutational analysis to study the role of genetic factors in pea adaptation to stresses during development its symbioses with Rhizobium and mycorrhizal fungi. - In: Wang, Y.P., Lin, M., Tian, Z.X., Elmerich, C., Newton, W.E. (ed.): Bacterial Nitrogen Fixation, Sustainable Agriculture and the Environment. Pp. 279–281. Springer, Dordrecht 2005.CrossRefGoogle Scholar
  40. Van Vliet, C., Anderson, C.R., Cobbett, C.S.: Copper-sensitive mutant of Arabidopsis thaliana. - Plant Physiol. 109: 871–878, 1995.CrossRefPubMedPubMedCentralGoogle Scholar
  41. Verkleij, J.A.C., Golan-Goldhirsh, A., Antosiewisz, D.M., Schwitzguebel, J.P., Schroder, P.: Dualities in plant tolerance to pollutants and their uptake and translocation to the upper plant parts. - Environ. exp. Bot. 67: 10–22, 2009.CrossRefGoogle Scholar
  42. Wang, Y., Zong, K., Jiang, L., Sun, J., Ren, Y., Sun, Z., Wen, C., Chen, X., Cao, S.: Characterization of an Arabidopsis cadmium-resistant mutant cdr3-1D reveals a link between heavy metal resistance as well as seed development and flowering. - Planta 233: 697–706, 2011.CrossRefPubMedGoogle Scholar
  43. Watanabe, A., Ito, H., Chiba, M., Ito, A., Shimizu, H., Fuji, S., Nakamura, S., Hattori, H., Chino, M., Satoh-Nagasawa, N., Takahashi, H., Sakurai, K., Akagi, H.: Isolation of novel types of Arabidopsis mutants with altered reactions to cadmium: cadmium-gradient agar plates are an effective screen for the heavy metal-related mutants. - Planta 232: 825–836, 2010.CrossRefPubMedGoogle Scholar
  44. Yang, X., Feng, Y., He, Z., Stoffella, P.J.: Molecular mechanisms of heavy metal hyperaccumulation and phytoremediation. - J. Trace Elem. Med. Bio. 18: 339–353, 2005.CrossRefGoogle Scholar
  45. Yang, X.E., Long, X.X., Ye, H.B., He, Z.L., Calvert D.V., Stoffella, P.J.: Cadmium tolerance and hyperaccumulation in a new Zn-hyperaccumulating plant species (Sedum alfredii Hance). - Plant Soil. 259: 181–189, 2004.CrossRefGoogle Scholar
  46. Zornoza, P., Vázquez, S., Esteban, E., Fernández-Pascual, M., Carpena, R.: Cadmium-stress in nodulated white lupin: strategies to avoid toxicity. - Plant Physiol. Biochem. 40: 1003–1009, 2002.CrossRefGoogle Scholar

Copyright information

© The Institute of Experimental Botany 2018

Authors and Affiliations

  • A. A. Belimov
    • 1
  • N. V. Malkov
    • 1
  • J. V. Puhalsky
    • 1
  • V. E. Tsyganov
    • 1
  • K. B. Bodyagina
    • 1
    • 2
  • V. I. Safronova
    • 1
  • K.-J. Dietz
    • 3
  • I. A. Tikhonovich
    • 1
    • 2
  1. 1.All-Russia Research Institute for Agricultural Microbiology, PushkinSt.-PetersburgRussia
  2. 2.Saint-Petersburg State UniversitySt.-PetersburgRussia
  3. 3.Bielefeld UniversityBielefeldGermany

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