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Intra-specific variation in zinc, cadmium and nickel hypertolerance and hyperaccumulation capacities in Noccaea caerulescens

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Abstract

Aims

The study aimed at characterizing the patterns of natural variation in the tolerance and accumulation capacities for zinc (Zn), cadmium (Cd), and nickel (Ni) between and within edaphic ecotypes of the Zn/Cd/Ni hyperaccumulator, Noccaea caerulescens.

Methods

Tolerance was assessed in a hydroponic ‘sequential exposure’ test, using the lowest concentration that completely arrested root growth as an end point. Accumulation was measured as the foliar metal concentration after six weeks of growth at 5 µM Zn, 2 µM Cd, or 1 µM Ni.

Results

Zn and Cd tolerance were positively correlated, and highest in the calamine ecotype. Ni tolerance was without significant ecotypic variation. The ultramafic ecotype was as Zn-tolerant as the non-metallicolous one, but much more sensitive to Cd. The accumulation capacities for Zn, Cd and Ni were all positively correlated and without significant ecotypic variation. Zn hyperaccumulation capacity was species-wide, but Cd and Ni hyperaccumulation capacities were lacking in four populations (all calamine).

Conclusions

There is considerable independent variation among populations regarding their Zn, Cd, and Ni accumulation capacities. This variation is most pronounced within the calamine ecotype, because some populations apparently had adopted an exclusion strategy for Zn or Cd hypertolerance, whereas others had not.

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References

  • Antonovics J, Bradshaw AD, Turner RG (1971) Heavy metal tolerance in plants. Adv Ecol Res 7:1–85

    Google Scholar 

  • Assunção AGL, Martins PD, De Folter S, Vooijs R, Schat H, Aarts MGM (2001) Elevated expression of metal transporter genes in three accessions of the metal hyperaccumulator Thlaspi caerulescens. Plant Cell Environ 24:217–226

    Google Scholar 

  • Assunção AGL, Schat H, Aarts MGM (2003a) Thlaspi caerulescens, an attractive model to study heavy metal tolerance in plants. New Phytol 159:351–360

    Google Scholar 

  • Assunção AGL, Ten Bookum WM, Nelissen HJM, Vooijs R, Schat H, Ernst WHO (2003b) A cosegregation analysis of zinc (Zn) accumulation and Zn tolerance in the Zn hyperaccumulator Thlaspi caerulescens. New Phytol 159:383–390

    Google Scholar 

  • Assunção AGL, Ten Bookum WM, Nelissen HJM, Vooijs R, Schat H, Ernst WHO (2003c) Differential metal-specific tolerance and accumulation patterns among Thlaspi caerulescens populations originating from different soil types. New Phytol 159:411–419

    Google Scholar 

  • Assunção AGL, Pieper B, Vromans J, Lindhout P, Aarts MGM, Schat H (2006) Construction of a genetic linkage map of Thlaspi caerulescens and quantitative trait loci analyses of zinc accumulation. New Phytol 170:21–32

    PubMed  Google Scholar 

  • Assunção AGL, Bleeker P, Ten Bookum WM, Vooijs R, Schat H (2008) Intraspecific variation of metal preference patterns for hyperaccumulation in Thlaspi caerulescens: evidence from binary exposures. Plant Soil 303:289–299

    Google Scholar 

  • Babst-Kostecka A. Schat H, Saumitou-Laprade P, Grodzińska K, Bourceaux A, Pauwels M, Frérot H (2018) Evolutionary dynamics of quantitative variation in an adaptive trait at the regional scale: the case of zinc hyperaccumulation in Arabidopsis halleri. Mol Ecol 27:3257–3273

  • Baker AJM (1981) Accumulators and excluders – strategies in the response of plants to heavy metals. J Plant Nutr 3:643–654

    CAS  Google Scholar 

  • Baker AJM, Brooks RR (1989) Terrestrial higher which hyperaccumulate metallic elements – a review of their distribution, ecology and phytochemistry. Biorecovery 1:81–126

    CAS  Google Scholar 

  • Boyd RS (2007) The defense hypothesis of elemental hyperaccumulation: status, challenges and new directions. Plant Soil 293:153–176

    CAS  Google Scholar 

  • Brooks RR (1994) Plants that hyperaccumulate heavy metals. In: Farago ME (ed) Plants and the chemical elements. VCH, Weinheim, pp 87–105

  • Cheruiyot DJ, Boyd RS, Moar WJ (2013) Exploring lower limits of plant elemental defense by cobalt, copper, nickel and zinc. J Chem Ecol 39:666–674

    PubMed  CAS  Google Scholar 

  • Craciun AR, Meyer C-L, Chen JG, Roosens N, de Groodt R, Hilson P, Verbruggen N (2012) Variation in HMA4 gene copy number and expression among Noccaea caerulescens populations presenting different levels of Cd tolerance and accumulation. J Exp Bot 63:4179–4189

    PubMed  CAS  Google Scholar 

  • Deniau AX, Pieper B, Ten Bookum WM, Lindhout P, Aarts MGM, Schat H (2006) QTL analysis of cadmium and zinc accumulation in the heavy metal hyperaccumulator Thlaspi caerulescens. Theor Appl Genet 113:907–920

    PubMed  CAS  Google Scholar 

  • Escarré J, Lefèbvre C, Gruber W, Leblanc M, Lepart J, Rivière Y, Delay B (2000) Zinc and Cd hyperaccumulation by Thlaspi caerulescens from metalliferous and non-metalliferous sites in the Mediterranian area: implications for phytoremediation. New Phytol 145:429–437

    Google Scholar 

  • Escarré J, Lefèbvre C, Frérot H, Mahieu S, Noret N (2013) Metal concentration and metal mass of metallicolous non metallicolous and serpentine Noccaea caerulescens populations, cultivated in different growth media. Plant Soil 370:197–221

    Google Scholar 

  • Frérot H, Lefèbvre C, Petit C, Collin C, Dos Santos A, Escarré J (2005) Zinc tolerance and hyperaccumulation in F1 and F2 offspring from intra and interecotype crosses of Thlaspi caerulescens. New Phytol 165:111–119

    PubMed  Google Scholar 

  • Gonneau C, Genevois N, Frérot H, Sirguey C, Sterckeman T (2014) Variation of trace metal accumulation, major nutrient uptake and growth parameters and their correlations in 22 populations of Noccaea caerulescens. Plant Soil 384:271–287

    CAS  Google Scholar 

  • Gonneau C, Noret N, Gode C, Frérot H, Sirguey C, Sterckeman T, Pauwels M (2017) Demographic history of the trace metal hyperaccumulator Noccaea caerulescens (J. Presl and C. Presl) F.K. Mey. in Western Europe. Mol Ecol 26:904–922

    PubMed  Google Scholar 

  • Halimaa P, Lin Y-F, Ahonen VA, Blande D, Clemens S, Gyenesei A, Häikiö E, Kärenlampi SO, Laiho A, Aarts MGM, Pursiheimo J-P, Schat H, Schmidt Н, Tuomainen M, Tervahauta AL (2014) Gene expression differences between Noccaea caerulescens ecotypes help to identify candidate genes for metal phytoremediation. Environ Sci Technol 48:3344–3353

    PubMed  CAS  Google Scholar 

  • Halimaa P, Blande D, Baltzi E, Aarts MGM, Granlund L, Keinänen M, Kärenlampi SO, Kozhevnikova AD, Peräniemi S, Schat H, Seregin IV, Tuomainen M, Tervahauta AL (2019) Transcriptional effects of cadmium on iron homeostasis differ in calamine accessions of Noccaea caerulescens. Plant J 97: 306–320

    PubMed  CAS  Google Scholar 

  • Hammond JP, Bowen HC, White PJ, Mills V, Pyke KA, Baker AJM, Whiting SN, May ST, Broadley MR (2006) A comparison of the Thlaspi caerulescens and Thlaspi arvense shoot transcriptomes. New Phytol 170:239–260

    PubMed  CAS  Google Scholar 

  • Hanikenne M, Talke IN, Haydon MJ, Lanz C, Nolte A, Motte P, Kroymann J, Weigel D, Krämer U (2008) Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453:391–395

    PubMed  CAS  Google Scholar 

  • O’Lochlainn S, Bowen HC, Fray RG, Hammond JP, King GJ, White PJ, Graham NS, Broadley MR (2011) Tandem quadruplication of HMA4 in the zinc (Zn) and cadmium (Cd) hyperaccumulator Noccaea caerulescens. PLoS One 6:e17814

    Google Scholar 

  • Lombi E, Zhao FJ, Dunham SJ, McGrath SP (2000) Cadmium accumulation in populations of Thlaspi caerulescens and Thlaspi goesingense. New Phytol 145:11–20

    CAS  Google Scholar 

  • Macnair MR (1983) The genetic control of copper tolerance in the yellow monkey flower, Mimulus guttatus. Heredity 50:283–293

    CAS  Google Scholar 

  • Macnair MR, Bert V, Huitson SB, Saumitou-Laprade P, Petit D (1999) Zinc tolerance and hyperaccumulation are genetically independent characters. Proc R Soc Lond B Biol Sci 266:2175–2179

    CAS  Google Scholar 

  • Meerts P, Van Isacker N (1997) Heavy metal tolerance and accumulation in metallicolous and non-metallicolous populations of Thlaspi caerulescens from continental Europe. Plant Ecol 133:221–231

    Google Scholar 

  • Merlot S, Hannibal L, Martins S, Martinelli L, Amir H, Lebrun M, Thomine S (2014) The metal transporter PgIREG1 from the hyperaccumulator Psychotria gabriellae is a candidate gene for nickel tolerance and accumulation. J Exp Bot 65:1551–1564

    PubMed  CAS  Google Scholar 

  • Meyer C-L, Kostecka AA, Saumitou-Laprade P, Creach A, Castric V, Pauwels M, Frérot H (2010) Variability of zinc tolerance among and within populations of the pseudometallophyte species Arabidopsis halleri and possible role of directional selection. New Phytol 185:130–142

    PubMed  CAS  Google Scholar 

  • Meyer C-L, Pauwels M, Briset L, Gode C, Salis P, Bourceau A, Souleman D, Frérot H, Verbruggen N (2016) Potential preadaptation to anthropogenic pollution: evidence from a common quantitative trait locus for zinc and cadmium tolerance in metallicolous and nonmetallicolous accessions of Arabidopsis halleri. New Phytol 212:934–943

    PubMed  CAS  Google Scholar 

  • Mizuno T, Usui K, Horie K, Nosaka S, Mizuno N, Obata H (2005) Cloning of three ZIP/Nramp transporter genes from a Ni hyperaccumulator plant Thlaspi japonicum and their Ni(II)-transport abilities. Plant Physiol Biochem 43:793–801

    PubMed  CAS  Google Scholar 

  • Mohtadi A, Ghaderian SM, Schat H (2012a) A comparison of lead accumulation and tolerance among heavy metal hyperaccumulating and non-hyperaccumulating metallophytes. Plant Soil 352:267–276

    CAS  Google Scholar 

  • Mohtadi A, Ghaderian SM, Schat H (2012b) Lead, zinc and cadmium accumulation from two metalliferous soils with contrasting calcium contents in heavy metal hyperaccumulating and non-hyperaccumulating metallophytes: a comparative study. Plant Soil 361:109–118

    CAS  Google Scholar 

  • Molitor M, Deschamps C, Gruber W, Meerts P (2005) Thlaspi caerulescens on non-metalliferous soil in Luxembourg: ecological niche and genetic variation in mineral element composition. New Phytol 165:503–512

    PubMed  Google Scholar 

  • Monna F, Petit C, Guillaumet J-P, Jouffroy-Bapicot I, Blanchot C, Dominik J, Losno R, Richard H, Leveque J, Chateau C (2004) History and environmental impact of mining activity in Celtic Aeduan Territory recorded in a peat bog (Morvan, France). Environ Sci Technol 38:667–673

    Google Scholar 

  • Nkrumah PN, Echevarria G, Erskine PD, van der Ent A (2018) Contrasting nickel and zinc hyperaccumulation in subspecies of Dichapetalum gelenioides from Southeast Asia. Sci Rep 8:9659

    PubMed  PubMed Central  Google Scholar 

  • Pauwels M, Frérot H, Bonnin I, Saumitou-Laprade P (2006) A broad-scale study of population differentiation for Zn tolerance in an emerging model species for tolerance study: Arabidopsis halleri (Brassicaceae). J Evol Biol 19:1838–1850

    PubMed  CAS  Google Scholar 

  • Plaza S, Tearall KL, Zhao F-J, Buchner P, McGrath SP, Hawkesford MJ (2007) Expression and functional analysis of metal transporter genes in two contrasting ecotypes of the hyperaccumulator Thlaspi caerulescens. J Exp Bot 58:1717–1728

    PubMed  CAS  Google Scholar 

  • Pollard AJ, Reeves RD, Baker AJM (2014) Facultative hyperaccumulation of heavy metals and metalloids. Plant Sci 217:8–17

    PubMed  Google Scholar 

  • Reeves RD, Schwartz C, Morel JL, Edmondson J (2001) Distribution and metal-accumulating behavior of Thlaspi caerulescens and associated metallophytes in France. Int J Phytoremediation 3:145–172

    CAS  Google Scholar 

  • Richau KH, Schat H (2009) Intraspecific variation of nickel and zinc accumulation and tolerance in the hyperaccumulator Thlaspi caerulescens. Plant Soil 314:253–262

    CAS  Google Scholar 

  • Richau KH, Kozhevnikova AD, Seregin IV, Vooijs R, Koevoets PLM, Smith JAC, Ivanov VB, Schat H (2009) Chelation by histidine inhibits the vacuolar sequestration of nickel in roots of the hyperaccumulator Thlaspi caerulescens. New Phytol 183:106–116

    PubMed  CAS  Google Scholar 

  • Schat H, Ten Bookum WM (1992) The genetic control of copper tolerance in Silene vulgaris. Heredity 68:219–229

    CAS  Google Scholar 

  • Schat H, Kuiper E, Ten Bookum WM, Vooijs R (1993) A general model for the genetic control of copper tolerance in Silene vulgaris – evidence from crosses between plants from different tolerant populations. Heredity 70:142–147

    CAS  Google Scholar 

  • Schat H, Llugany M, Bernard R (2000) Metal-specific patterns of tolerance, uptake, and transport of heavy metals in hyperaccumulating and non-hyperaccumulating metallophytes. In: Terry N, Banuelos G (eds) Phytoremediation of contaminated soils and water. CRC Press LLC, Boca Raton, pp 171–188

    Google Scholar 

  • Seregin IV, Erlikh NT, Kozhevnikova AD (2014) Nickel and zinc accumulation capacities and tolerance to these metals in the excluder Thlaspi arvense and the hyperaccumulator Noccaea caerulescens. Russ J Plant Physiol 61:204–214

    CAS  Google Scholar 

  • Seregin IV, Kozhevnikova AD, Zhukovskaya NV, Schat H (2015) Cadmium tolerance and accumulation in excluder Thlaspi arvense and various accessions of hyperaccumulator Noccaea caerulescens. Russ J Plant Physiol 62:837–846

    CAS  Google Scholar 

  • Sharma SS, Schat H, Vooijs R, Van Heerwaarden LM (1999) 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 18:348–355

    CAS  Google Scholar 

  • Sokal RR, Rohlf FJ (1981) Biometry, 2nd edn. Freeman WH & Co, San Francisco

    Google Scholar 

  • Stein RJ, Höreth S, de Melo JRF, Syllwasschy L, Lee G, Garbin ML, Clemens S, Krämer U (2016) Relationships between soil and leaf mineral composition are element-specific, environment-dependent and geographically structured in the emerging model Arabidopsis halleri. New Phytol 213:1274–1286

    PubMed  PubMed Central  Google Scholar 

  • Sterckeman T, Cazes Y, Gonneau C, Sirguey C (2017) Phenotyping 60 populations of Noccaea caerulescens provides a broader knowledge of variation in traits of interest for phytoextraction. Plant Soil 418:523–540

    CAS  Google Scholar 

  • Talke IN, Hanikenne M, Kramer U (2006) Zinc-dependent transcriptional control, transcriptional deregulation, and higher gene copy number for genes in metal homeostasis of the hyperaccumulator Arabidopsis halleri. Plant Physiol 142:148–167

    PubMed  PubMed Central  CAS  Google Scholar 

  • Van de Mortel JE, Villanueva LA, Schat H, Kwekkeboom J, Coughlan S, Moerland PD, van Themaat EVL, Koornneef M, Aarts MGM (2006) Large expression differences in genes for iron and zinc homeostasis, stress response, and lignin synthesis distinguish roots of Arabidopsis thaliana and the related metal hyperaccumulator Thlaspi caerulescens. Plant Physiol 142:1127–1147

    PubMed  PubMed Central  Google Scholar 

  • Van der Ent A, Baker AJM, Reeves RD, Pollard AJ, Schat H (2013) Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant Soil 362:319–334

    Google Scholar 

  • Verbruggen N, Hermans C, Schat H (2009) Molecular mechanisms of metal hyperaccumulation in plants. New Phytol 181:759–776

    PubMed  CAS  Google Scholar 

  • Visioli G, Gulli M, Marmiroli N (2014) 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 105:10–17

    CAS  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

    PubMed  CAS  Google Scholar 

  • Xing JP, Jiang RF, Ueno D, Ma JF, Schat H, McGrath SP, Zhao FJ (2008) Variation in root-to-shoot translocation of cadmium and zinc among different accessions of the hyperaccumulators Thlaspi caerulescens and Thlaspi praecox. New Phytol 178:315–325

    PubMed  CAS  Google Scholar 

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Acknowledgements

The authors wish to thank Mathilde Mousset, Thibault Sterckeman, Celestino Quintela-Sabarís, Petra Kidd, Oihana Barrutía and Sylvain Merlot for supplying seeds of N. caerulescens, Hélène Frérot-Pauwels for seeds of A. lyrata and A. halleri, Takafumi Mizuno for seeds of N. japonicum, and Rudo Verweij, Rob Broekman, Richard van Logtestijn, Riet Vooijs and Sandy Goette for technical assistance. This work was partially supported by the grants from the Russian Foundation for Basic Research (RFBR, № 19-04-00369) and from the international scientific program GDRI LOCOMET (Transport, localization and complexation of metals in hyperaccumulating plants) funded by The National Centre for Scientific Research, France; and partially by the Ministry of Science and Higher Education of the Russian Federation (state assignment №АААА-А19-119040290058-5).

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H.S. designed and performed the experiments and statistical analyses. A.D.K., I.V.S., and H.S. performed the mineral analyses. All authors contributed to the writing of the manuscript.

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Correspondence to Henk Schat.

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Responsible Editor: Fangjie Zhao.

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Figure S1

N. caerulescens root system staining with carbon for the sequential exposure test. A ̶ roots immediately after staining; B-D ̶ roots after 4 days of incubation on half-strength Hoagland`s nutrient solution following the staining with carbon; newly grown white root apices are marked with white arrowheads (DOCX 3597 kb)

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Kozhevnikova, A.D., Seregin, I.V., Aarts, M.G.M. et al. Intra-specific variation in zinc, cadmium and nickel hypertolerance and hyperaccumulation capacities in Noccaea caerulescens. Plant Soil 452, 479–498 (2020). https://doi.org/10.1007/s11104-020-04572-7

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