Cd-Fe interactions: Comparison of the Effects of Iron Deficiency and Cadmium on Growth and Photosynthetic Performance in Poplar

Abstract

To check the importance of Cd-induced iron deficiency in Cd stress, symptoms of Cd stress were compared with those of iron deficiency or the combination of these two stresses. Poplar plants grown in hydroponics with Fe-EDTA (e) or Fe-citrate (c) up to four-leaf stage were treated for two weeks either by the withdrawal of iron (Fedef), or supplying 10 μM Cd(NO3)2 in the presence (Cad) or absence of an iron source (Fedef + Cad). Cadmium and iron content of leaves developing under the stress was in the order of cCad>eCad>cFedef+Cad and cCad≈ eFedef ≈ cFedef + Cad < eCad < cFedef, respectively. Growth inhibition was much stronger in Cad than Fedef plants. The inhibitory effects on CO2 fixation, maximal and actual efficiency of PSII, chlorophyll synthesis, as well as the stimulation of the accumulation of violaxanthin cycle components and increase in non-photochemical quenching were the strongest in cFedef+Cad plants, otherwise these parameters changed parallel to the iron deficiency of leaves. Tendency of changes in thylakoid composition were similar under Cad treatments and strong iron deficiency: particularly PSI and LHCII decreased. Therefore, the development of the photosynthetic apparatus under Cd stress was mainly influenced by the Cd-induced strong iron deficiency, while leaf growth was affected primarily by the presence of Cd.

References

  1. 1.

    Alcántara, E., Romera, F. J., Cañete, M., de la Guardia, M. D. (1994) Effects of heavy metals on both induction and function of root Fe(III) reductase in Fe-deficient cucumber (Cucumis sativus L.) plants. J. Exp. Bot. 45, 1893–1898.

    Google Scholar 

  2. 2.

    Ambler, J. E., Brown, J. C., Gauch, H. G. (1970) Effect of zinc on translocation of iron in soybean plants. Plant Physiol. 46, 320–323.

    CAS  PubMed  PubMed Central  Google Scholar 

  3. 3.

    Barceló, J., Poschenrieder, C. (1990) Plant water relations as affected by heavy metal stress: a review. J. Plant Nutr. 13, 1–37.

    Google Scholar 

  4. 4.

    Belkhodja, R., Morales, F., Quílez, R., López-Millán, A. F., Abadía, A., Abadía, J. (1998) Iron deficiency causes changes in chlorophyll fluorescence due to the reduction in the dark of the photosystem II acceptor side. Photosynth. Res. 56, 265–276.

    CAS  Google Scholar 

  5. 5.

    Chow, W. S., Lee, H. Y., Park, Y. I., Park, Y. M., Hong, Y. N., Anderson, J. M. (2002) The role of inactive photosystem-II-mediated quenching in a last-ditch community defence against high light stress in vivo. Philos. Trans. R. Soc. London 357B, 1441–1450.

    Google Scholar 

  6. 6.

    Clemens, S. (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88, 1707–1719.

    CAS  PubMed  Google Scholar 

  7. 7.

    DalCorso, G., Farinati, S., Maistri, S., Furini, A. (2008) How plants cope with cadmium: Staking all on metabolism and gene expression. J. Int. Plant Biol. 50, 1268–1280.

    CAS  Google Scholar 

  8. 8.

    Fagioni, M., D’Amici, G. M., Timperio, A. M., Zolla, L. (2009) Proteomic analysis of multiprotein complexis in the thylakoid membrane upon cadmium treatment. J. Proteome Res. 8, 310–326.

    CAS  PubMed  Google Scholar 

  9. 9.

    Faller, P., Kienzler, K., Krieger-Liszkay, A. (2004) Mechanism of Cd2+ toxicity: Cd2+ inhibits photoactivation of photosystem II by competitive binding to the essential Ca2+ site. Biochim. Biophys. Acta 1706, 158–164.

    Google Scholar 

  10. 10.

    Fodor, F., Cseh, E., Varga, A., Záray, Gy. (1998) Lead uptake, distribution, and remobilization in cucumber. J. Plant Nutr. 21, 1363–1373.

    CAS  Google Scholar 

  11. 11.

    Fodor, F., Gáspár, L., Morales, F., Gogorcena, Y., Lucena, J. J., Cseh, E., Kröpfl, K., Abadía, J., Sárvári, É. (2005) The effect of two different iron sources on iron and cadmium allocation in cadmium exposed poplar plants (Populus alba L.). Tree Physiol. 25, 1173–1180.

    CAS  PubMed  Google Scholar 

  12. 12.

    Gratao, P. L., Polle, A., Lea, P. J., Azevedo, R. A. (2005) Making the life of heavy metal-stressed plants a little easier. Funct. Plant Physiol. 32, 481–494.

    CAS  Google Scholar 

  13. 13.

    Hodoshima, H., Enomoto, Y., Shoji, K., Shimada, H., Goto, F., Yoshihara, T. (2007) Differential regulation of cadmium-inducible expression of iron-deficiency-responsive genes in tobacco and barley. Physiol. Plant. 129, 622–634.

    CAS  Google Scholar 

  14. 14.

    Horváth, G., Droppa, M., Oravecz, Á., Raskin, V. I., Marder, J. B. (1996) Formation of the photosynthetic apparatus during greening. Planta 199, 238–243.

    Google Scholar 

  15. 15.

    Iametti, S., Uhlmann, H., Sala, N., Bernhardt, R., Raggi, E., Bonomi, F. (1996) Reversible, non-denaturing metal substitution in bovine adrenodoxin and spinach ferredoxin and the different reactivities of [2Fe-2S]-cluster-containing proteins. Eur. J. Biochem. 239, 818–826.

    CAS  PubMed  Google Scholar 

  16. 16.

    Kieffer, P., Dommes, J., Hoffmann, L., Hausman, J-F., Renaut J. (2008) Quantitative changes in protein expression of cadmium-exposed poplar plants. Proteomics 8, 2514–2530.

    CAS  PubMed  Google Scholar 

  17. 17.

    Kieffer, P., Planchon, S., Oufir, M., Ziebel, J., Dommes, J., Hoffmann, L., Hausman, J-F., Renaut J. (2009) Combining proteomics and metabolite analyses to unravel cadmium stress-response in poplar leaves. J. Proteome Res. 8, 400–417.

    CAS  PubMed  Google Scholar 

  18. 18.

    Korshunova, Y. O., Eide, D., W., Clark, G., Guerinot, M. L., Pakrasi, H. B. (1999) The IRT 1 protein from Arabidopsis thaliana is a metal transporter with a broad substrate range. Plant Mol. Biol. 40, 37–44.

    CAS  PubMed  Google Scholar 

  19. 19.

    Krupa, Z., Baszyński, T. (1995) Some aspects of heavy metals toxicity towards photosynthetic apparatus–direct and indirect effects on light and dark reactions. Acta Physiol. Plant. 17, 177–190.

    CAS  Google Scholar 

  20. 20.

    Kučera, T., Horáková, H., Šonská, A. (2008) Toxic metal ions in photoautotrophic organisms. Photosynthetica 46, 481–489.

    Google Scholar 

  21. 21.

    Küpper, H., Küpper, F., Spiller, M. (1998) In situ detection of heavy metal substituted chlorophylls in water plants. Photosynth. Res. 58, 123–133.

    Google Scholar 

  22. 22.

    Laganowsky, A., Gómez, S. M., Whitelegge, J. P., Nishio, J. N. (2009) Hydroponics on a chip: Analysis of the Fe deficient Arabidopsis thylakoid membrane proteome. J. Proteomics 72, 397–415.

    CAS  PubMed  Google Scholar 

  23. 23.

    Láng, F., Sárvári, É., Szigeti, Z. (1985) Apparatus and method for rapid determination of photosynthetic CO2-fixation of leaves. Biochem. Physiol. Pflanzen 180, 333–336.

    Google Scholar 

  24. 24.

    Morales, F., Abadía, A., Abadía, J. (1998) Photosynthesis, quenching of chlorophyll fluorescence and thermal energy dissipation in iron-deficient sugar beet leaves. Austr. J. Plant Physiol. 25, 403–412.

    CAS  Google Scholar 

  25. 25.

    Myśliwa-Kurdziel, B., Strzałka, K. (2002) Influence of metals on biosynthesis of photosynthetic pigments. In: Prasad, M. N. V., Strzałka, K. (eds) Physiology and Biochemistry of Metal Toxicity and Tolerance in Plants. Kluwer Academic Publ., The Netherlands, pp. 201–227.

    Google Scholar 

  26. 26.

    Padmaja, K., Prasad, D. D. K., Prasad, A. R. K. (1990) Inhibition of chlorophyll synthesis in Phaseolus vulgaris L. seedlings by cadmium acetate. Photosynthetica 24, 399–405.

    CAS  Google Scholar 

  27. 27.

    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.

    CAS  PubMed  Google Scholar 

  28. 28.

    Porra, R. J., Thompson, W. A., Kriedemann, P. E. (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim. Biophys. Acta 975, 384–394.

    CAS  Google Scholar 

  29. 29.

    Prasad, M. N. V. (1995) Cadmium toxicity and tolerance in vascular plants. Environ. Exp. Bot. 35, 525–545.

    CAS  Google Scholar 

  30. 30.

    Qureshi, M. I., D’Amici, G. M., Fagioni, M., Rinalducci, S., Zolla, L. (2010) Iron stabilizes thylakoid protein–pigment complexes in Indian mustard during Cd-phytoremediation as revealed by BN-SDSPAGE and ESI-MS/MS. J. Plant Physiol. 167, 761–770.

    CAS  PubMed  Google Scholar 

  31. 31.

    Rengel, Z., Römheld, V. (2000) Root exudation and Fe uptake and transport in wheat genotypes differing in tolerance to Zn deficiency. Plant Soil 222, 25–34.

    CAS  Google Scholar 

  32. 32.

    Rodecap, K. D., Tingey, D. T., Lee, E. H. (1994) Iron nutrition influence on cadmium accumulation by Arabidopsis thaliana (L.) Heynh. J. Environ. Qual. 23, 239–246.

    CAS  Google Scholar 

  33. 33.

    Sanità di Toppi, L., Gabbrielli, R. (1999) Response to cadmium in higher plants. Environ. Exp. Bot. 41, 105–130.

    Google Scholar 

  34. 34.

    Sárvári, É. (2005) Effects of heavy metals on chlorophyll-protein complexes in higher plants: Causes and consequences. In: Pessarakli, M. (ed.) Handbook of Photosynthesis. CRC Press, Boca Raton, USA, pp. 865–888.

    Google Scholar 

  35. 35.

    Sárvári, É., Fodor, F., Cseh, E., Varga, A,, Záray, Gy., Zolla, L. (1999) Relationship between changes in ion content of leaves and chlorophyll-protein composition in cucumber under Cd and Pb stress. Z. Naturforsch. 54C, 746–753.

    Google Scholar 

  36. 36.

    Sárvári, É., Nyitrai, P. (1994) Separation of chlorophyll-protein complexes by Deriphat polyacrylamide gradient gel electrophoresis. Electrophoresis 15, 1067–1071.

    Google Scholar 

  37. 37.

    Siedlecka, A., Krupa, Z. (1999) Cd/Fe interaction in higher plants–its consequences for the photosynthethic apparatus. Photosynthetica 36, 321–331.

    CAS  Google Scholar 

  38. 38.

    Sigfridsson, K. G. V., Bernat, G., Mamedov, F., Styring, S. (2004) Molecular interference of Cd2+ with Photosystem II. Biochim. Biophys. Acta 1659, 19–31.

    CAS  PubMed  Google Scholar 

  39. 39.

    Solti, Á., Gáspár, L., Mészáros, I., Szigeti, Z., Lévai, L., Sárvári, É. (2008) Impact of iron supply on the kinetics of recovery of photosynthesis in Cd-stressed poplar (Populus glauca). Ann. Bot. 102, 771–782.

    CAS  PubMed  PubMed Central  Google Scholar 

  40. 40.

    Solti, Á., Szűcs, J., Basa, B., Sárvári, É. (2009) Functional and organisational change of photosystem II in poplar thylakoids under Cd stress (Dissipative PSII centres in Cd treated poplar thylakoids). Cer. Res. Commun. 37S, 525–528.

    Google Scholar 

  41. 41.

    Stiborová, M. (1988) Cd2+ ions affect the quaternary structure of ribulose-1,5-bisphosphate carboxylase from barley leaves. Biochem. Physiol. Pflanzen 183, 371–378.

    Google Scholar 

  42. 42.

    Stobart, A. K., Griffiths, W. T., Ameen-Bukhari, I., Sherwood, R. P. (1985) The effect of Cd2+ on the biosynthesis of chlorophyll in leaves of barley. Physiol. Plant. 63, 293–298.

    CAS  Google Scholar 

  43. 43.

    Timperio, A. M., D’Amici, G. M., Barta, C., Loreto, F., Zolla, L. (2007) Proteomics, pigment composition, and organization of thylakoid membranes in iron-deficient spinach leaves. J. Exp. Bot. 58, 3695–3710.

    CAS  PubMed  Google Scholar 

  44. 44.

    Tóth, V. R., Mészáros, I., Veres, Sz., Nagy, J. (2002) Effects of the available nitrogen on the photosynthetic activity and xanthophyll cycle pool of maize in field. J. Plant Physiol. 159, 627–634.

    Google Scholar 

  45. 45.

    Tziveleka, L., Kaldis, A., Hegedüs, A., Kissimon, J., Prombona, A., Horváth, G., Argyroudi-Akoyunoglou, J. (1999) The effect of Cd on chlorophyll and light-harvesting complex II biosynthesis in greening plants. Z. Naturforsch. 54C, 740–745.

    Google Scholar 

  46. 46.

    Vallee, B. L. (1990) Zinc coordination, function, and structure of zinc enzymes and other proteins. Biochemistry 29, 5647–5659.

    CAS  Google Scholar 

  47. 47.

    Van Assche, F., Clijsters, H. (1990) Effects of metals on enzyme activity in plants. Plant Cell Environ. 13, 195–206.

    Google Scholar 

  48. 48.

    Varga, A., Záray, Gy., Fodor, F., Cseh, E. (1997) Study of interaction of iron and lead during their uptake process in wheat roots by total reflection X-ray fluorescence spectrometry. Spectrochim. Acta 52B, 1027–1032.

    CAS  Google Scholar 

  49. 49.

    Webster, E, A., Gadd, G. M. (1996) Cadmium replaces calcium in the cell wall of Ulva lactuca. BioMetals 9, 241–244.

    CAS  Google Scholar 

  50. 50.

    Xiao, H., Yin, L., Xu, X., Li, T., Han, Z. (2008) The iron-regulated transporter, MbNRAMP1, isolated from Malus baccata is involved in Fe, Mn and Cd trafficking. Ann. Bot. 102, 881–889.

    CAS  PubMed  PubMed Central  Google Scholar 

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Correspondence to Éva Sárvári.

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Sárvári, É., Gáspár, L., Solti, Á. et al. Cd-Fe interactions: Comparison of the Effects of Iron Deficiency and Cadmium on Growth and Photosynthetic Performance in Poplar. BIOLOGIA FUTURA 61, 136–148 (2010). https://doi.org/10.1556/ABiol.61.2010.Suppl.14

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Keywords

  • Cadmium
  • chlorophyll-protein complexes
  • fluorescence induction
  • iron deficiency
  • poplar