Abstract
Aims
The aim of the present study was to compare lead accumulation and tolerance among heavy metal hyperaccumulating and non-hyperaccumulating metallophytes.
Methods
To this purpose, we compared Pb tolerance and accumulation in hydroponics among calamine and non-calamine populations of Silene vulgaris, Noccaea caerulescens, and Matthiola flavida. We established the effects of Ca on Pb tolerance and accumulation in M. flavida, and measured exchangeable soil Pb and Ca at two calamine sites.
Results
Results revealed that calamine populations of S. vulgaris and N. caerulescens were Pb hypertolerant, but the calamine M. flavida population was not. Pb hyperaccumulation capacity was exclusively found in one of the calamine N. caerulescens populations.
Conclusions
1) Pb hypertolerance is sometimes lacking in metallophyte populations from strongly Pb-enriched soil, probably due to a relatively high level of exchangeable soil Ca, 2) Ca effectively counteracts Pb uptake and Pb toxicity, 3) The tendency to hyperaccumulate Pb is a population-specific phenomenon in N. caerulescens, 4) Pb hypertolerance in N. caerulescens is not necessarily associated with a tendency to hyperaccumulate Pb, 5) apparent natural Pb hyperaccumulation in M. flavida is not reproducible in hydroponics, probably due to the absence of air-born contamination in laboratory experiments.
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References
Antonovics J, Bradshaw AD, Turner RG (1971) Heavy metal tolerance in plants. Adv Ecol Res 7:1–85
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 analysis of zinc accumulation. New Phytol 170:21–32
Assunção AGL, Ten Bookum WM, Nelissen HJM, Vooijs R, Schat H, Ernst WHO (2003a) Differential metal-specific tolerance and accumulation patterns among Thlaspi caerulescens originating from different soil types. New Phytol 159:411–419
Assunção AGL, Ten Bookum WM, Nelissen HJM, Vooijs R, Schat H, Ernst WHO (2003b) A co-segregation analysis of zinc (Zn) accumulation and Zn tolerance in the Zn hyperaccumulator Thlaspi caerulescens. New Phytol 159:383–390
Baker AJM (1981) Accumulators and excluders—strategies in the response of plants to heavy metals. J Plant Nutr 3:643–654
Baker AJM (1987) Metal tolerance. New Phytol 106:93–111
Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements—a review of their distribution, ecology and phytochemistry. Biorecovery 1:81–126
Baker AJM, Reeves RD, Hajar ASM (1994) Heavy metal accumulation and tolerance in British populations of the metallophyte Thlaspi caerulescens J. and C. Pressl (Brassicaceae). New Phytol 127:61–68
Brown G, Brinkmann K (1992) Heavy-metal tolerance in Festuca ovina L. from contaminated sites in the Eifel Mountains, Germany. Plant Soil 143:239–247
Clemens S (2001) Molecular mechanisms of plant metal homeostasis and tolerance. Planta 212:475–486
Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88:1707–1719
Courbot M, Willems G, Motte P, Arvidson S, Roosens N, Saumitou-Laprade P, Verbruggen N (2007) A major quantitative trait locus for cadmium tolerance in Arabidopsis halleri colocalizes with HMA4, a gene encoding a heavy metal ATPase. Plant Physiol 144:1052–1065
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
Ernst WHO (1982) Schwermetallpflanzen. In: Kinzel H (ed) Pflanzenökologie und Mineralstoffwechsel. E. Ulmer Verlag, Stuttgart, pp 473–505
Faucon MP, Shutsha MN, Meerts P (2007) Revisiting copper and cobalt concentrations in supposed hyperaccumulators from SC Africa: influence of washing and metal concentrations in soil. Plant Soil 301:29–36
Gartside DW, McNeilly T (1974) Potential for evolution of heavy-metal tolerance in plants. II. Copper tolerance in normal populations of different plant species. Heredity 32:335–348
Ghaderian SM, Hemmat GR, Reeves RD, Baker AJM (2007) Accumulation of lead and zinc by plants colonizing a metal mining area in Central Iran. J Appl Bot Food Qual 81:145–150
Hanikenne M, Nouet C (2011) Metal hyperaccumulation and hypertolerance: a model for plant evolutionary genomics. Curr Opin Plant Biol 14:1–8
Jack E, Hakvoort HWJ, Reumer A, Verkleij JAC, Schat H, Ernst WHO (2007) Real-time PCR analysis of metallothionein expression in metallicolous and non-metallicolous populations of Silene vulgaris (Moench) Garcke. Environ Exp Bot 59:84–91
Jiménez-Ambriz G, Petit C, Bourrié I, Dubois S, Olivieri I, Ronce O (2007) Life history variation in the heavy metal tolerant plant Thlaspi caerulescens growing in a network of contaminated and noncontaminated sites in southern France: role of gene flow, selection and phenotypic plasticity. New Phytol 173:199–215
Krämer U (2010) Metal hyperaccumulation in plants. Ann Rev Plant Biol 61:517–534
Macnair MR (1993) The genetics of metal tolerance in vascular plants. New Phytol 124:541–559
Macnair MR (2002) Within and between population genetic variation for zinc accumulation in Arabidopsis halleri. New Phytol 155:59–66
McNaught SJ, Folsom TC, Lee T, Park F, Price C, Roeder D, Schmitz J, Stockwell C (1974) Heavy metal tolerance in Typha latifolia without evolution of tolerant races. Ecology 55:1163–1165
Meyer CL, Kostecka AA, Saumitou-Laprade P, Créach A, Castric V, Pauwels M, Frérot H (2010) Variability of zinc tolerance among and within populations of the pseudometallophyte Arabidopsis halleri and the possible role of directional selection. New Phytol 185:130–142
Pauwels M, Frérot H, Bonnin I, Saumitou-Laprade P (2006) A broad-scale analysis of population differentiation for Zn tolerance in an emerging model species for tolerance study: Arabidopsis halleri. J Evol Biol 19:1838–1850
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 3:275–283
Sarwar GR (2002) Flora of Pakistan. University of Karachi, Missouri Botanical Press
Schat H, Ten Bookum WM (1992a) Metal-specificity of metal tolerance syndromes in higher plants. In: Baker AJM, Proctor J, Reeves RD (eds) The vegetation of ultramafic soils. Intercept, Andover, pp 337–352
Schat H, Ten Bookum WM (1992b) Genetic control of copper tolerance in Silene vulgaris. Heredity 68:219–229
Schat H, Vooijs R (1997) Multiple tolerance and co-tolerance to heavy metals in Silene vulgaris. New Phytol 136:489–496
Schat H, Vooijs R, Kuiper E (1996) Identical major gene loci for heavy metal tolerances that have independently evolved in different local populations and subspecies of Silene vulgaris. Evolution 50:1888–1895
Simon E (1978) Heavy metals in soils, vegetation development and heavy metal tolerance in plant populations from metalliferous areas. New Phytol 81:175–188
Sokal RR, Rolph FJ (1981) Biometry, 2nd edn. Freeman and Company, San Francisco
Verbruggen N, Hermans C, Schat H (2009) Molecular mechanisms of metal hyperaccumulation in plants. New Phytol 181:759–776
Verkleij JAC, Prast JE (1989) Cadmium tolerance and co-tolerance in Silene vulgaris (Moench.) Garcke [= S. cucubalus (L.) Wib.]. New Phytol 111:637–645
Zha HG, Jiang RF, Zhao FJ, Vooijs R, Schat H, Barker JHA, McGrath SP (2004) Co-segregation analysis of cadmium and zinc accumulation in Thlaspi caerulescens interecotypic crosses. New Phytol 163:299–312
Acknowledgements
We gratefully acknowledge a scholarship to A. Mohtadi from the Ministry of Science, Research and Technology of Iran (MSRT) and Graduate School of the University of Isfahan.
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Responsible Editor: Juan Barcelo.
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Mohtadi, A., Ghaderian, S.M. & Schat, H. A comparison of lead accumulation and tolerance among heavy metal hyperaccumulating and non-hyperaccumulating metallophytes. Plant Soil 352, 267–276 (2012). https://doi.org/10.1007/s11104-011-0994-5
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DOI: https://doi.org/10.1007/s11104-011-0994-5