Log in

Correlated Variation of the Zn Accumulation and Tolerance Capacities among Populations and Ecotypes of the Zn Hyperaccumulator, Noccaea caerulescens

  • RESEARCH PAPERS
  • Published:
Russian Journal of Plant Physiology Aims and scope Submit manuscript

Abstract

In this work, a comparative analysis of zinc (Zn) accumulation by the excluder Microthlaspi perfoliatum (L.) F.K. Mey, the hyperaccumulator Noccaea japonicum (H. Boissieu) F.K. Mey from ultramafic (serpentine) soil and plants from 19 populations of the hyperaccumulator Noccaea caerulescens F.K. Mey originating from ultramafic, calamine and non-metalliferous soils was carried out. The seedlings were grown for 2 weeks on half-strength Hoagland’s solution at 2 μM ZnSO4, followed by incubation for 6 weeks at 5 μM ZnSO4 (these Zn concentrations were non-toxic for all the populations of all species). The Zn concentration in the roots and shoots was determined by atomic absorption spectrophotometry. In M. perfoliatum, the Zn concentration in the roots was significantly higher than in the shoots, whereas in the hyperaccumulators, N. japonicum and N. caerulescens, the Zn concentrations in both organs were in most cases similar or higher in the shoots. Within N. caerulescens the greatest differences in Zn accumulation in roots and shoots were found among the calamine populations whereas the smallest differences were found among the ultramafic populations. Zn accumulation in roots per unit dry weight decreased in the following order: Les Avinières ≈ St-Baudille ≈ Viviez ≈ Le Coulet ≈ Le Puy de Wolf > Cira > Puente Basadre > Moravskoslezské ≈ Monte Prinzera > St‑Fé-lix-de-Pallières ≈ Prémanon > La Calamine > Le Bleymard > Krušné Hory ≈ Kuopio > Prayon > Wilwerwiltz ≈ Jean Arsac ≈ Plombières. The value of the translocation factor (TF) was the lowest in the excluder M. perfoliatum. In N. japonicum, TF did not significantly differ from the ultramafic populations of N. caerulescens. Among populations of N. caerulescens, the mean TF values varied to a large extent. The highest TF value (5.83) was obtained for Prayon and the lowest value (0.37) for Les Avinières, both belonging to the calamine ecotype. No correlation was found between the Zn concentration in the roots and the Zn concentration in the shoots in N. caerulescens. A significant negative correlation was found between the Zn accumulation in the roots and plant Zn tolerance estimated by the root growth test, which indicates that root Zn tolerance in N. caerulescens might depend, to some extent, on the capacity to restrict the accumulation of Zn in the root, mainly through restricting its uptake into the root. The difference in root Zn tolerance between the calamine and non-metallicolous ecotypes seems to be largely explained by an enhanced Zn sequestration capacity in the calamine ecotype, compared to the non-metallicolous one.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.

Similar content being viewed by others

REFERENCES

  1. Brooks, R.R., Lee, J., Reeves, R.D., and Jaffré, T., Detection of nickeliferous rocks by analysis of herbarium specimens of indicator plants, J. Geochem. Explor., 1977, vol. 7, p. 49.

    Article  CAS  Google Scholar 

  2. Reeves, R.D., Baker, A.J., Jaffré, T., Erskine, P.D., Echevarria, G., and van der Ent, A., A global database for plants that hyperaccumulate metal and metalloid trace elements, New Phytol., 2018, vol. 218, p. 407.

    Article  PubMed  Google Scholar 

  3. Verbruggen, N., Hermans, C., and Schat, H., Molecular mechanisms of metal hyperaccumulation in plants, New Phytol., 2009, vol. 181, p. 759.

    Article  CAS  PubMed  Google Scholar 

  4. Krämer, U., Metal hyperaccumulation in plants, Ann. Rev. Plant Biol., 2010, vol. 61, p. 517.

    Article  CAS  Google Scholar 

  5. Assunção, A.G., Bookum, W.M., Nelissen, H.J., Vooijs, R., Schat, H., and Ernst, W.H., Differential metal-specific tolerance and accumulation patterns among Thlaspi caerulescens populations originating from different soil types, New Phytol., 2003, vol. 159, p. 411.

    Article  PubMed  CAS  Google Scholar 

  6. Assunção, A.G., Schat, H., and Aarts, M.G., Thlaspi caerulescens, an attractive model species to study heavy metal hyperaccumulation in plants, New Phytol., 2003, vol. 159, p. 351.

    Article  PubMed  CAS  Google Scholar 

  7. Richau, K.H., Kozhevnikova, A.D., Seregin, I.V., Vooijs, R., Koevoets, P.L., Smith, J.A., Ivanov, V.B., and Schat, H., Chelation by histidine inhibits the vacuolar sequestration of nickel in roots of the hyperaccumulator Thlaspi caerulescens, New Phytol., 2009, vol. 183, p. 106.

    Article  CAS  PubMed  Google Scholar 

  8. Gonneau, C., Genevois, N., Frérot, H., Sirguey, C., and Sterckeman, T., Variation of trace metal accumulation, major nutrient uptake and growth parameters and their correlations in 22 populations of Noccaea caerulescens, Plant Soil, 2014, vol. 384, p. 271.

    Article  CAS  Google Scholar 

  9. Seregin, I.V., Erlikh, N.T., and Kozhevnikova, A.D., Nickel and zinc accumulation capacities and tolerance to these metals in the excluder Thlaspi arvense and the hyperaccumulator Noccaea caerulescens, Russ. J. Plant Physiol., 2014, vol. 61, p. 204.

    Article  CAS  Google Scholar 

  10. Seregin, I.V., Kozhevnikova, A.D., Zhukovskaya, N.V., and Schat, H., Cadmium tolerance and accumulation in excluder Thlaspi arvense and various accessions of hyperaccumulator Noccaea caerulescens, Russ. J. Plant Physiol., 2015, vol. 62, p. 837.

    Article  CAS  Google Scholar 

  11. Kozhevnikova, A.D., Seregin, I.V., and Schat, H., Accumulation of nickel by excluder Thlaspi arvense and hyperaccumulator Noccaea caerulescens upon short-term and long-term exposure, Russ. J. Plant Physiol., 2020, vol. 67, p. 303.

    Article  CAS  Google Scholar 

  12. Sterckeman, T., Cazes, Y., Gonneau, C., and Sirguey, C., Phenoty** 60 populations of Noccaea caerulescens provides a broader knowledge of variation in traits of interest for phytoextraction, Plant Soil, 2017, vol. 418, p. 523.

    Article  CAS  Google Scholar 

  13. Kozhevnikova, A.D., Seregin, I.V., Erlikh, N.T., Shevyreva, T.A., Andreev, I.M., Verweij, R., Schat, H., Histidine-mediated xylem loading of zinc is a species-wide character in Noccaea caerulescens, New Phytol., 2014, vol. 203, p. 508.

    Article  CAS  PubMed  Google Scholar 

  14. Kozhevnikova, A.D., Seregin, I.V., Aarts, M.G., and Schat, H., Intra-specific variation in zinc, cadmium and nickel hypertolerance and hyperaccumulation capacities in Noccaea caerulescens, Plant Soil, 2020, vol. 452, p. 479.

    Article  CAS  Google Scholar 

  15. Callahan, D.L., Baker, A.J., Kolev, S.D., and Wedd, A.G., Metal ion ligands in hyperaccumulating plants, J. Biol. Inorg. Chem., 2006, vol. 11, p. 2.

    Article  CAS  PubMed  Google Scholar 

  16. Pollard, A.J., Powell, K.D., Harper, F.A., and Smith, J.A.C., The genetic basis of metal hyperaccumulation in plants, Crit. Rev. Plant Sci., 2002, vol. 21, p. 539.

    Article  CAS  Google Scholar 

  17. Pollard, A.J., Reeves, R.D., and Baker, A.J.M., Facultative hyperaccumulation of heavy metals and metalloids, Plant Sci., 2014, vol. 217, p. 8.

    Article  PubMed  CAS  Google Scholar 

  18. Seregin, I.V. and Kozhevnikova, A.D., Low-molecular-weight ligands in plants: role in metal homeostasis and hyperaccumulation, Photosynth. Res., 2020. https://doi.org/10.1007/s11120-020-00768-1

  19. Shen, Z.G., Zhao, F.J., and McGrath, S.P., Uptake and transport of zinc in the hyperaccumulator Thlaspi caerulescens and the non-hyperaccumulator Thlaspi ochroleucum, Plant Cell Environ., 1997, vol. 20, p. 898.

    Article  CAS  Google Scholar 

  20. Marschner, H., Mineral Nutrition of Higher Plants, San Diego: Elsevier, 1995, 2nd ed.

    Google Scholar 

  21. Escarré, J., Lefèbvre, C., Gruber, W., Leblanc, M., Lepart, J., Rivière, Y., and Delay, B., Zinc and cadmium hyperaccumulation by Thlaspi caerulescens from metalliferous and nonmetalliferous sites in the Mediterranean area: implications for phytoremediation, New Phytol., 2000, vol. 145, p. 429.

    Article  PubMed  Google Scholar 

  22. Escarré, J., Lefèbvre, C., Frérot, H., Mahieu, S., and Noret, N., Metal concentration and metal mass of metallicolous, non metallicolous and serpentine Noccaea caerulescens populations, cultivated in different growth media, Plant Soil, 2013, vol. 370, p. 197.

    Article  CAS  Google Scholar 

  23. Hanikenne, M. and Nouet, C., Metal hyperaccumulation and hypertolerance: a model for plant evolutionary genomics, Curr. Opin. Plant Biol., 2011, vol. 14, p. 252.

    Article  CAS  PubMed  Google Scholar 

  24. Stein, R.J., Höreth, S., de Melo, J.R., Syllwasschy, L., Lee, G., Garbin, M.L., Clemens, S., and Krämer, U., Relationships between soil and leaf mineral composition are element-specific, environment-dependent and geographically structured in the emerging model Arabidopsis halleri, New Phytol., 2017, vol. 213, p. 1274.

    Article  CAS  PubMed  Google Scholar 

  25. Assunção, A.G., Ten Bookum, W.M., Nelissen, H.J., Vooijs, R., Schat, H., and Ernst, W.H., A cosegregation analysis of zinc (Zn) accumulation and Zn tolerance in the Zn hyperaccumulator Thlaspi caerulescens, New Phytol., 2003, vol. 159, p. 383.

    Article  PubMed  CAS  Google Scholar 

  26. Assunção, A.G.L., Pieper, B., Vromans, J., Lindhout, P., Aarts, M.G.M., and Schat, H., Construction of a genetic linkage map of Thlaspi caerulescens and quantitative trait loci analyses of zinc accumulation, New Phytol., 2006, vol. 170, p. 21.

    Article  PubMed  CAS  Google Scholar 

  27. Deniau, A.X., Pieper, B., Ten Bookum, W.M., Lindhout, P., Aarts, M.G.M., and Schat, H., QTL analysis of cadmium and zinc accumulation in the heavy metal hyperaccumulator Thlaspi caerulescens, Theor. Appl. Genet., 2006, vol. 113, p. 907.

    Article  CAS  PubMed  Google Scholar 

  28. Macnair, M.R., Bert, V., Huitson, S.B., Saumitou-Laprade, P., and Petit, D., Zinc tolerance and hyperaccumulation are genetically independent characters, Proc. R. Soc. London, Ser. B, 1999, vol. 266, p. 2175.

    Article  CAS  Google Scholar 

  29. Bert, V., Meerts, P., Saumitou-Laprade, P., Salis, P., Gruber, W., and Verbruggen, N., Genetic basis of Cd tolerance and hyperaccumulation in Arabidopsis halleri, Plant Soil, 2003, vol. 249, p. 9.

    Article  CAS  Google Scholar 

  30. Hanikenne, M., Talke, I.N., Haydon, M.J., Lanz, C., Nolte, A., Motte, P., Kroymann, J., Weigel, D., and Krämer, U., Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4, Nature, 2008, vol. 453, p. 391.

    Article  CAS  PubMed  Google Scholar 

  31. Lin, Y.F. and Aarts, M.G.M., The molecular mechanism of zinc and cadmium stress response in plants, Cell Mol. Life Sci., 2012, vol. 69, p. 3187.

    Article  CAS  PubMed  Google Scholar 

  32. Merlot, S., de la Torre, V.S., and Hanikenne, M., Physiology and molecular biology of trace element hyperaccumulation, in Agromining: Farming for Metals—Extracting Unconventional Resources Using Plants, van der Ent, A., Ed., Cham: Springer-Verlag, 2018, p. 93.

    Google Scholar 

  33. Mizuno, T., Usui, K., Horie, K., Nosaka, S., Mizuno, N., and Obata, H., Cloning of three ZIP/Nramp transporter genes from a Ni hyperaccumulator plant Thlaspi japonicum and their Ni(II)-transport abilities, Plant Physiol. Biochem., 2005, vol. 43, p. 793.

    Article  CAS  PubMed  Google Scholar 

  34. Sokal, R.R. and Rohlf, F.J., Biometry, San Francisco: W.H. Freeman, 1981, 2nd ed.

    Google Scholar 

  35. Reeves, R.D., Schwartz, C., Morel, J.L., and Edmondson, J., Distribution and metal-accumulating behavior of Thlaspi caerulescens and associated metallophytes in France, Int. J. Phytorem., 2001, vol. 3, p. 145.

    Article  CAS  Google Scholar 

  36. Kazemi-Dinan, A., Thomaschky, S., Stein, R.J., Krämer, U., and Müller, C., Zinc and cadmium hyperaccumulation act as deterrents towards specialist herbivores and impede the performance of a generalist herbivore, New Phytol., 2014, vol. 202, p. 628.

    Article  CAS  PubMed  Google Scholar 

  37. Muehe, E.M., Weigold, P., Adaktylou, I.J., Planer-Friedrich, B., Kraemer, U., Kappler, A., and Behrens, S., Rhizosphere microbial community composition affects cadmium and zinc uptake by the metal-hyperaccumulating plant Arabidopsis halleri, Appl. Environ. Microbiol., 2015, vol. 81, p. 2173.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Plaza, S., Weber, J., Pajonk, S., Thomas, J., Talke, I.N., Schellenberg, M., Pradervand, S., Burla, B., Geisler, M., Martinoia, E., and Krämer, U., Wounding of Arabidopsis halleri leaves enhances cadmium accumulation that acts as a defense against herbivory, BioMetals, 2015, vol. 28, p. 521.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Sharma, S.S., Schat, H., Vooijs, R., and van Heerwaarden, L.M., Combination toxicology of copper, zinc and cadmium in binary mixtures: concentration-dependent antagonistic, nonadditive, and synergistic effects on root growth in Silene vulgaris, Environ. Toxicol. Chem., 1999, vol. 18, p. 348.

    Article  CAS  Google Scholar 

  40. Assunção, A.G., Martins, P.D., De Folter, S., Vooijs, R., Schat, H., and Aarts, M.G.M., Elevated expression of metal transporter genes in three accessions of the metal hyperaccumulator Thlaspi caerulescens, Plant Cell Environ., 2001, vol. 24, p. 217.

    Article  Google Scholar 

  41. Mohseni, R., Ghaderian, S.M., Ghasemi, R., and Schat, H., Differential effects of iron starvation and iron excess on nickel uptake kinetics in two Iranian nickel hyperaccumulators, Odontarrhena bracteata and Odontarrhena inflate, Plant Soil, 2018, vol. 428, p. 153.

    Article  CAS  Google Scholar 

  42. Mohseni, R., Ghaderian, S.M., and Schat, H., Nickel uptake mechanisms in two Iranian nickel hyperaccumulators, Odontarrhena bracteata and Odontarrhena inflate, Plant Soil, 2019, vol. 434, p. 263.

    Article  CAS  Google Scholar 

  43. Plaza, S., Tearall, K.L., Zhao, F.J., Buchner, P., McGrath, S.P., and Hawkesford, M.J., Expression and functional analysis of metal transporter genes in two contrasting ecotypes of the hyperaccumulator Thlaspi caerulescens, J. Exp. Bot., 2007, vol. 58, p. 1717.

    Article  CAS  PubMed  Google Scholar 

  44. Halimaa, P., Lin, Y.-F., Ahonen, V.H., Blane, D., Clemens, S., Gyenesei, A., Häikiö, E., Kärenlampi, S.O., Laiho, A., Aarts, M.G.M., Pursiheimo, G.-M., Schat, H., Schmidt, H., Tuomainen, M.H., and Tervahauta, A.I., Gene expression differences between Noccaea caerulescens ecotypes help identifying candidate genes for metal phytoremediation, Environ. Sci. Technol., 2014, vol. 48, p. 3344.

    Article  CAS  PubMed  Google Scholar 

  45. Pence, N.S., Larsen, P.B., Ebbs, S.D., Letham, D.L., Lasat, M.M., Garvin, D.F., Eide, D., and Kochian, L.V., The molecular physiology of heavy metal transport in the Zn/Cd hyperaccumulator Thlaspi caerulescens, Proc. Natl. Acad. Sci. U.S.A., 2000, vol. 97, p. 4956.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Milner, M.J., Craft, E., Yamaji, N., Koyama, E., Ma, J.F., and Kochian, L.V., Characterization of the high affinity Zn transporter from Noccaea caerulescens, NcZNT1, and dissection of its promoter for its role in Zn uptake and hyperaccumulation, New Phytol., 2012, vol. 195, p. 113.

    Article  CAS  PubMed  Google Scholar 

  47. Visioli, G., Gullì, M., and Marmiroli, N., Noccaea caerulescens populations adapted to grow in metalliferous and non-metalliferous soils: Ni tolerance, accumulation and expression analysis of genes involved in metal homeostasis, Environ. Exp. Bot., 2014, vol. 105, p. 10.

    Article  CAS  Google Scholar 

  48. Assunção, A.G.L., Bleeker, P., Ten Bookum, W.M., Vooijs, R., and Schat, H., Intraspecific variation of metal preference patterns for hyperaccumulation in Thlaspi caerulescens: evidence from binary exposures, Plant Soil, 2008, vol. 303, p. 289.

    Article  CAS  Google Scholar 

  49. van der Ent, A., Baker, A.J.M., Reeves, R.D., Pollard, A.J., and Schat, H., Hyperaccumulators of metal and metalloid trace elements: facts and fiction, Plant Soil, 2013, vol. 362, p. 319.

    Article  CAS  Google Scholar 

  50. Hussain, D., Haydon, M.J., Wang, Y., Wong, E., Sherson, S.M., Young, J., Camakaris, J., Harper, J.F., and Cobbett, C.S., P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis, Plant Cell, 2004, vol. 16, p. 1327.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Verret, F., Gravot, A., Auroy, P., Leonhardt, N., David, P., Nussaume, L., Vavasseur, A., and Richaud, P., Overexpression of AtHMA4 enhances root-to-shoot translocation of zinc and cadmium and plant metal tolerance, FEBS Lett., 2004, vol. 576, p. 306.

    Article  CAS  PubMed  Google Scholar 

  52. Craciun, A.R., Meyer, C.L., Chen, J., Roosens, N., De Groodt, R., Hilson, P., and Verbruggen, N., Variation in HMA4 gene copy number and expression among Noccaea caerulescens populations presenting different levels of Cd tolerance and accumulation, J. Exp. Bot., 2012, vol. 63, p. 4179.

    Article  CAS  PubMed  Google Scholar 

  53. Talke, I.N., Hanikenne, M., and Krämer, U., Zinc-dependent global transcriptional control, transcriptional deregulation, and higher gene copy number for genes in metal homeostasis of the hyperaccumulator Arabidopsis halleri, Plant Physiol., 2006, vol. 142, p. 148.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Lochlainn, S.Ó., Bowen, H.C., Fray, R.G., Hammond, J.P., King, G.J., White, P.J., Graham, N.S., and Broadley, M.R., Tandem quadruplication of HMA4 in the zinc (Zn) and cadmium (Cd) hyperaccumulator Noccaea caerulescens, PloS One, 2011, vol. 6, p. e17814.

    Article  CAS  Google Scholar 

  55. Bernard, C., Roosens, N., Czernic, P., Lebrun, M., and Verbruggen, N., A novel CPx-ATPase from the cadmium hyperaccumulator Thlaspi caerulescens, FEBS Lett., 2004, vol. 569, p. 140.

    Article  CAS  PubMed  Google Scholar 

  56. Roux, C., Castric, V., Pauwels, M., Wright, S.I., Saumitou-Laprade, P., and Vekemans, X., Does speciation between Arabidopsis halleri and Arabidopsis lyrata coincide with major changes in a molecular target of adaptation? PLoS One, 2011, vol. 6, p. e26872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Weber, M., Harada, E., Vess, C., von Roepenack-Lahaye, E., and Clemens, S., Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors, Plant J., 2004, vol. 37, p. 269.

    Article  CAS  PubMed  Google Scholar 

  58. Hammond, J.P., Bowen, H.C., White, P.J., Mills, V., Pyke, K.A., Baker, A.J.M., Whiting, S.N., May, S.T., and Broadley, M.R., A comparison of the Thlaspi caerulescens and Thlaspi arvense shoot transcriptomes, New Phytol., 2006, vol. 170, p. 239.

    Article  CAS  PubMed  Google Scholar 

  59. van de Mortel, J.E., Villanueva, L.A., Schat, H., Kwekkeboom, J., Coughlan, S., Moerland, P.D., van Themaat, E.V., Koornneef, M., and Aarts, M.G.M., Large expression differences in genes for iron and zinc homeostasis, stress response, and lignin biosynthesis distinguish roots of Arabidopsis thaliana and the related metal hyperaccumulator Thlaspi caerulescens, Plant Physiol., 2006, vol. 142, p. 1127.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. de Knecht, J.A., van Dillen, M., Koevoets, P.L., Schat, H., Verkleij, J.A., and Ernst, W.H., Phytochelatins in cadmium-sensitive and cadmium-tolerant Silene vulgaris (chain length distribution and sulfide incorporation), Plant Physiol., 1994, vol. 104, p. 255.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Harmens, H., Den Hartog, P.R., Bookum, W.M.T., and Verkleij, J.A., Increased zinc tolerance in Silene vulgaris (Moench) Garcke is not due to increased production of phytochelatins, Plant Physiol., 1993, vol. 103, p. 1305.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Frérot, H., Lefèbvre, C., Petit, C., Collin, C., Dos Santos, A., and Escarré, J., Zinc tolerance and hyperaccumulation in F1 and F2 offspring from intra and interecotype crosses of Thlaspi caerulescens, New Phytol., 2005, vol. 165, p. 111.

    Article  PubMed  CAS  Google Scholar 

Download references

ACKNOWLEDGMENTS

The authors wish to thank Mark Aarts, Mathilde Mousset, Thibault Sterckeman, Celestino Quintela-Sabarís, Petra Kidd, Oihana Barrutía and Sylvain Merlot for supplying the seeds of N. caerulescens, Takafumi Mizuno for the seeds of N. japonicum, and Rudo Verweij, Rob Broekman, Richard van Logtestijn, Riet Vooijs, and Sandy Goette for technical assistance. The authors thank the Ministry of Science and Higher Education of the Russian Federation (state assignment no. 121040800153-1) for the maintenance of growth and research facilities at the Timiryazev Institute of Plant Physiology, Russian Academy of Sciences.

Funding

This work was supported by the Russian Science Foundation (grant no. 21-14-00028). The studies of Zn accumulation in Noccaea japonicum were supported by the Ministry of Science and Higher Education of the Russian Federation (state assignment no. 121040800153-1).

Author information

Authors and Affiliations

Authors

Contributions

Authors I.V. Seregin and A.D. Kozhevnikova contributed equally to the work.

Corresponding author

Correspondence to I. V. Seregin.

Ethics declarations

Conflict of interests. The authors declare that they have no conflicts of interest.

Statement on the welfare of humans or animals. This article does not contain any studies involving animals performed by any of the authors.

Additional information

Abbreviations: Ci—Cira; СМА—Col du Mas de l’Ayre; Co—Le Coulet; JA—Jean Arsac; КН—Krušné Hory; Ku—Kuopio; LA—Les Avinières; LB—Le Bleymard; LC—La Calamine; LE—Lellingen; MP—Monte Prinzera; MS—Moravskoslezské; PB—Puente Basadre; PdW—Le Puy de Wolf; Pl—Plombières; Po—Pontaut; Pr—Prayon; Prem—Prémanon; SB—St-Baudille; SF—St-Félix-de-Pallières; SLM—St-Laurent-le-Minier (previously Ganges); Vi—Viviez; Wi—Wilwerwiltz (populations of the hyperaccumulator Noccaea caerulescens); TF—translocation factor.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Seregin, I.V., Kozhevnikova, A.D. & Schat, H. Correlated Variation of the Zn Accumulation and Tolerance Capacities among Populations and Ecotypes of the Zn Hyperaccumulator, Noccaea caerulescens . Russ J Plant Physiol 68 (Suppl 1), S26–S36 (2021). https://doi.org/10.1134/S1021443721070128

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1021443721070128

Keywords:

Navigation