Variability of zinc tolerance among and within populations of the pseudometallophyte species Arabidopsis halleri and possible role of directional selection
Abstract
We estimated the level of quantitative polymorphism for zinc (Zn) tolerance in neighboring metallicolous and nonmetallicolous populations of Arabidopsis halleri and tested the hypothesis that divergent selection has shaped this polymorphism. A short-term hydroponic test was used to capture the quantitative polymorphism present between edaphic types, among and within populations. We measured six morphological and physiological traits on shoots and roots to estimate the response of A. halleri to Zn. In order to assess the adaptive value of Zn tolerance polymorphism, we compared differentiation of quantitative traits with that of molecular markers. Zinc tolerance of metallicolous populations was, on average, higher than that of nonmetallicolous populations according to the morphological and physiological traits measured. Phenotypic variability within edaphic types was very high and mainly explained by polymorphism among individuals within populations. Genetic differentiation for photosystem II yield of leaves (a measure of photosynthetic efficiency) was greater than the differentiation for microsatellite and thus, probably shaped by divergent selection. Overall, these results suggest that, in the sampled populations, Zn tolerance has been increased in metallicolous populations through selection on standing genetic variation within local nonmetallicolous ancestral populations.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
A. halleri shows species-wide Zn and Cd hypertolerance, with significant variation among its various populations.
“In addition, A. halleri shows species-wide Zn and Cd hypertolerance, with significant variation among its various populations (Pauwels et al., 2006; Meyer et al., 2010; Corso et al., 2018).”
From Plant hyperaccumulators: a state-of-the-art review on mechanism of heavy metal transport and sequestration (2025) · cites this paper as Meyer et al., 2010
Cites
Nonparametric Statistics for the Behavioral Sciences
Guitton, H., & Siegel, S. (1958) · Revue économique · doi:10.2307/3498751 · Cited by 35,281 · see citing works
ESTIMATING F -STATISTICS FOR THE ANALYSIS OF POPULATION STRUCTURE
Weir, B. S., & Cockerham, C. C. (1984) · Evolution · doi:10.1111/j.1558-5646.1984.tb05657.x · Cited by 18,909 · see citing works
Genty, B., Briantais, J., & Baker, N. R. (1989) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/s0304-4165(89)80016-9 · Cited by 8,741 · see citing works
FSTAT (Version 1.2): A Computer Program to Calculate F-Statistics
Goudet, J. (1995) · Journal of Heredity · doi:10.1093/oxfordjournals.jhered.a111627 · Cited by 7,639 · see citing works
Broadley, M. R., White, P. J., Hammond, J. P., Zelko, I., & Lux, A. (2007) · New Phytologist · doi:10.1111/j.1469-8137.2007.01996.x · Cited by 2,112 · see citing works
Adaptation from standing genetic variation
BARRETT, R., & SCHLUTER, D. (2008) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2007.09.008 · Cited by 2,091 · see citing works
Molecular Signatures of Natural Selection
Nielsen, R. (2005) · Annual Review of Genetics · doi:10.1146/annurev.genet.39.073003.112420 · Cited by 1,644 · see citing works
Phytoremediation of Contaminated Soil and Water
(1999) · CRC Press eBooks · doi:10.1201/9781439822654 · Cited by 1,525 · see citing works
Heavy metal tolerance of plants
Bothe, H. (2014) · Acta Biologica Cracoviensia. Series Zoologia · Cited by 1,008 · see citing works
Reznick, D. N., & Ghalambor, C. K. (2001) · Contemporary issues in genetics and evolution · doi:10.1007/978-94-010-0585-2_12 · Cited by 743 · see citing works
A Single Amino Acid Mutation Contributes to Adaptive Beach Mouse Color Pattern
Hoekstra, H. E., Hirschmann, R. J., Bundey, R. A., Insel, P. A., & Crossland, J. P. (2006) · Science · doi:10.1126/science.1126121 · Cited by 716 · see citing works
Küpper, H., Lombi, E., Zhao, F.-J., & McGrath, S. P. (2000) · Planta · doi:10.1007/s004250000366 · Cited by 685 · see citing works
Convergence and parallelism reconsidered: what have we learned about the genetics of adaptation?
ARENDT, J., & Reznick, D. N. (2007) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2007.09.011 · Cited by 630 · see citing works
THE MEASUREMENT OF TOLERANCE TO EDAPHIC FACTORS BY MEANS OF ROOT GROWTH
Wilkins, D. A. (1978) · New Phytologist · doi:10.1111/j.1469-8137.1978.tb01595.x · Cited by 552 · see citing works
van de Mortel, J. E., Almar Villanueva, L., Schat, H., Kwekkeboom, J., Coughlan, S., Moerland, P. D., Ver Loren van Themaat, E., Koornneef, M., & Aarts, M. G. M. (2006) · Plant Physiology · doi:10.1104/pp.106.082073 · Cited by 547 · see citing works
Assunção, A. G. L., Martins, P. D. C., de Folter, S., Vooijs, R., Schat, H., & Aarts, M. G. M. (2001) · Plant Cell & Environment · doi:10.1046/j.1365-3040.2001.00666.x · Cited by 402 · see citing works
Baryla, A., Carrier, P., Franck, F., Coulomb, C., Sahut, C., & Havaux, M. (2001) · Planta · doi:10.1007/s004250000439 · Cited by 393 · see citing works
Evolutionary inference from <i>Q</i> <sub>ST</sub>
WHITLOCK, M. C. (2008) · Molecular Ecology · doi:10.1111/j.1365-294x.2008.03712.x · Cited by 384 · see citing works
Whiting, S. N., Reeves, R. D., Richards, D., Johnson, M. S., Cooke, J. A., Malaisse, F., Paton, A., Smith, J. A. C., Angle, J. S., Chaney, R. L., et al. (2004) · Restoration Ecology · doi:10.1111/j.1061-2971.2004.00367.x · Cited by 355 · see citing works
Assunção, A. G. L., Martins, P. D. C., De Folter, S., Vooijs, R., Schat, H., & Aarts, M. G. M. (2001) · Plant, Cell & Environment · doi:10.1111/j.1365-3040.2001.00666.x · Cited by 350 · see citing works
Discriminant function analysis with nonindependent data: consequences and an alternative
Mundry, R., & Sommer, C. (2007) · Animal Behaviour · doi:10.1016/j.anbehav.2006.12.028 · Cited by 325 · see citing works
Küpper, H., Aravind, P., Leitenmaier, B., Trtílek, M., & Šetlík, I. (2007) · New Phytologist · doi:10.1111/j.1469-8137.2007.02139.x · Cited by 321 · see citing works
Courbot, M., Willems, G., Motte, P., Arvidsson, S., Roosens, N., Saumitou-Laprade, P., & Verbruggen, N. (2007) · Plant Physiology · doi:10.1104/pp.106.095133 · Cited by 303 · see citing works
Self-citationAssunção, A. G. L., Bookum, W. M. T., Nelissen, H. J. M., Vooijs, R., Schat, H., & Ernst, W. H. O. (2003) · New Phytologist · doi:10.1046/j.1469-8137.2003.00819.x · Cited by 275 · see citing works
The potential for evolution of heavy metal tolerance in plants
Walley, K. A., Khan, M. S. I., & Bradshaw, A. D. (1974) · Heredity · doi:10.1038/hdy.1974.40 · Cited by 257 · see citing works
Bert, V., Bonnin, I., Saumitou‐Laprade, P., De Laguérie, P., & Petit, D. (2002) · New Phytologist · doi:10.1046/j.1469-8137.2002.00432.x · Cited by 257 · see citing works
Self-citationA novel CPx‐ATPase from the cadmium hyperaccumulator <i>Thlaspi caerulescens</i>
Bernard, C., Roosens, N., Czernic, P., Lebrun, M., & Verbruggen, N. (2004) · FEBS Letters · doi:10.1016/j.febslet.2004.05.036 · Cited by 248 · see citing works
Populations of Agrostis tenuis Resistant to Lead and Zinc Poisoning
Bradshaw, A. D. (1952) · Nature · doi:10.1038/1691098a0 · Cited by 245 · see citing works
The potential for evolution of heavy metal tolerance in plants
Wu, L., Bradshaw, A. D., & Thurman, D. A. (1975) · Heredity · doi:10.1038/hdy.1975.21 · Cited by 232 · see citing works
BERT, V., MACNAIR, M. R., DE LAGUERIE, P., SAUMITOU‐LAPRADE, P., & PETIT, D. (2000) · New Phytologist · doi:10.1046/j.1469-8137.2000.00634.x · Cited by 225 · see citing works
Self-citationGenetic control of copper tolerance in Silene vulgaris
Schat, H., & Bookum, W. M. T. (1992) · Heredity · doi:10.1038/hdy.1992.35 · Cited by 200 · see citing works
Zinc tolerance and hyperaccumulation are genetically independent characters
Macnair, M. R., Bert, V., Huitson, S. B., Saumitou‐Laprade, P., & Petit, D. (1999) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1999.0905 · Cited by 196 · see citing works
Self-citationWillems, G., Dräger, D. B., Courbot, M., Godé, C., Verbruggen, N., & Saumitou-Laprade, P. (2007) · Genetics · doi:10.1534/genetics.106.064485 · Cited by 182 · see citing works
Self-citationBoulding, E. G., & Hay, T. K. (2001) · Heredity · doi:10.1046/j.1365-2540.2001.00829.x · Cited by 177 · see citing works
Taxonomy and Phylogeny of Arabidopsis (Brassicaceae)
Al-Shehbaz, I. A., & O’Kane, S. L. (2002) · The Arabidopsis Book · doi:10.1199/tab.0001 · Cited by 168 · see citing works
Schat, H., Vooijs, R., & Kuiper, E. (1996) · Evolution · doi:10.1111/j.1558-5646.1996.tb03576.x · Cited by 166 · see citing works
Meerts, P., & van isacker, N. (1997) · Plant Ecology · doi:10.1023/a:1009717619579 · Cited by 164 · see citing works
Pauwels, M., Saumitou‐Laprade, P., Holl, A.-C., Petit, D., & Bonnin, I. (2005) · Molecular Ecology · doi:10.1111/j.1365-294x.2005.02739.x · Cited by 148 · see citing works
Self-citationThe genetic control of copper tolerance in the yellow monkey flower, Mimulus guttatus
Macnair, M. R. (1983) · Heredity · doi:10.1038/hdy.1983.30 · Cited by 137 · see citing works
Ambriz, G. J., Petit, C., Bourrié, I., Dubois, S., Olivieri, I., & Ronce, O. (2006) · New Phytologist · doi:10.1111/j.1469-8137.2006.01923.x · Cited by 121 · see citing works
Vekemans, X., & Lefebvre, C. (1997) · Journal of Evolutionary Biology · doi:10.1046/j.1420-9101.1997.10020175.x · Cited by 120 · see citing works
Multiple tolerance and co‐tolerance to heavy metals in Silene vulgaris: a co‐segregation analysis
Schat, H., & Vooijs, R. (1997) · New Phytologist · doi:10.1046/j.1469-8137.1997.00756.x · Cited by 109 · see citing works
Pauwels, M., Frérot, H., Bonnin, I., & Saumitou-laprade, P. (2006) · Journal of Evolutionary Biology · doi:10.1111/j.1420-9101.2006.01178.x · Cited by 104 · see citing works
Self-citationUsing Arabidopsis to explore zinc tolerance and hyperaccumulation
Roosens, N. H. C., Willems, G., & Saumitou‐Laprade, P. (2008) · Trends in Plant Science · doi:10.1016/j.tplants.2008.02.006 · Cited by 94 · see citing works
Self-citationThe Genetics of Metal Tolerance and Accumulation in Higher Plants
Macnair, M. R., Tilstone, G. H., & Smith, S. E. (2020) · CRC Press eBooks · doi:10.1201/9780367803148-13 · Cited by 90 · see citing works
Mengoni, A., Barabesi, C., Gonnelli, C., Galardi, F., Gabbrielli, R., & Bazzicalupo, M. (2001) · Molecular Ecology · doi:10.1046/j.0962-1083.2001.01336.x · Cited by 88 · see citing works
O’Kane, S. L., & Al-Shehbaz, I. A. (2003) · Annals of the Missouri Botanical Garden · doi:10.2307/3298545 · Cited by 85 · see citing works
The effects of zinc contamination from electricity pylons – evolution in a replicated situation
Al-Hiyaly, S. A. K., McNeilly, T., & Bradshaw, A. D. (1988) · New Phytologist · doi:10.1111/j.1469-8137.1988.tb00297.x · Cited by 82 · see citing works
Schat, H., Kuiper, E., Bookum, W. M. T., et al. (1993) · Heredity · doi:10.1038/hdy.1993.23 · Cited by 80 · see citing works
Systematics and evolutionary history of heavy metal tolerant Thlaspi caerulescens in Western Europe
Koch, М. A., Mummenhoff, K., & Hurka, H. (1998) · Biochemical Systematics and Ecology · doi:10.1016/s0305-1978(98)00057-x · Cited by 78 · see citing works
Cho, M., Chardonnens, A. N., & Dietz, K. (2003) · New Phytologist · doi:10.1046/j.1469-8137.2003.00746.x · Cited by 76 · see citing works
Rossum, F. V., Bonnin, I., Fénart, S., Pauwels, M., Petit, D., & Saumitou‐Laprade, P. (2004) · Molecular Ecology · doi:10.1111/j.1365-294x.2004.02314.x · Cited by 73 · see citing works
Self-citationMeyer, C.-L., Vitalis, R., Saumitou‐Laprade, P., & Castric, V. (2009) · Molecular Ecology · doi:10.1111/j.1365-294x.2009.04159.x · Cited by 72 · see citing works
Self-citationDechamps, C., Lefèbvre, C., Noret, N., & Meerts, P. (2006) · New Phytologist · doi:10.1111/j.1469-8137.2006.01884.x · Cited by 63 · see citing works
Llaurens, V., Castric, V., Austerlitz, F., et al. (2008) · Molecular Ecology · doi:10.1111/j.1365-294x.2007.03683.x · Cited by 55 · see citing works
Self-citationRELATIONSHIPS BETWEEN TOLERANCE TO HEAVY METALS IN AGROSTIS CAPILLARIS L. (A. TENUIS SIBTH.)
And, M. O. H., & Nicholls, M. K. (1984) · New Phytologist · doi:10.1111/j.1469-8137.1984.tb06107.x · Cited by 52 · see citing works
Hypostatic modifiers cause variation in degree of copper tolerance in Mimulus guttatus
Smith, S. E., & Macnair, M. R. (1998) · Heredity · doi:10.1046/j.1365-2540.1998.00351.x · Cited by 52 · see citing works
Galardi, F., Corrales, I., Mengoni, A., Pucci, S., Barletti, L., Barzanti, R., Arnetoli, M., Gabbrielli, R., & Gonnelli, C. (2007) · Environmental and Experimental Botany · doi:10.1016/j.envexpbot.2006.12.011 · Cited by 46 · see citing works
FRENCKELL‐INSAM, B. A. K. V., & Hutchinson, T. C. (1993) · New Phytologist · doi:10.1111/j.1469-8137.1993.tb03903.x · Cited by 34 · see citing works
Roosens, N. H. C., Willems, G., Godé, C., Courseaux, A., & Saumitou‐Laprade, P. (2007) · Plant and Soil · doi:10.1007/s11104-007-9383-5 · Cited by 33 · see citing works
Self-citation(2004) · Mycological Research · doi:10.1017/s0953756204219669 · Cited by 33 · see citing works
Waldmann, P., García‐Gil, M. R., & Sillanpää, M. J. (2005) · Heredity · doi:10.1038/sj.hdy.6800672 · Cited by 32 · see citing works
Metal‐Tolerant Plants: An Evolutionary Perspective
Macnair, M. R., & Baker, A. J. M. (1994) · doi:10.1002/9783527615919.ch3 · Cited by 28 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Cd speciation and localization in the hyperaccumulator Arabidopsis halleri
Huguet, S., Bert, V., Laboudigue, A., Barthès, V., Isaure, M.-P., Llorens, I., Schat, H., & Sarret, G. (2012) · Environmental and Experimental Botany · doi:10.1016/j.envexpbot.2012.03.011 · Cited by 124 · see citing works
Frérot, H., Faucon, M., Willems, G., Godé, C., Courseaux, A., Darracq, A., Verbruggen, N., & Saumitou‐Laprade, P. (2010) · New Phytologist · doi:10.1111/j.1469-8137.2010.03295.x · Cited by 85 · see citing works
Self-citationLow-molecular-weight ligands in plants: role in metal homeostasis and hyperaccumulation
Seregin, I. V., & Kozhevnikova, A. D. (2021) · Photosynthesis Research · doi:10.1007/s11120-020-00768-1 · Cited by 73 · see citing works
Bhat, B. A., Rather, M. A., Bilal, T., Nazir, R., Qadir, R. U., & Mir, R. A. (2025) · Frontiers in Plant Science · doi:10.3389/fpls.2025.1631378 · Cited by 68 · see citing works
- Authors
- Meyer, C., Kostecka, A. A., Saumitou‐Laprade, P., Créach, A., Castric, V., Pauwels, M., & Frérot, H.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Corresponding author
- Meyer, Claire‐Lise
- Venue
- New Phytologist
- Publisher
- Wiley
- Published
- 2009-10-23
- Volume
- 185
- Issue
- 1
- Pages
- 130-142
- ISSN
- 0028-646X (ISSN-L)
- 1469-8137
- OpenAlex
- W2028735706
- Cited by
- 110
- References
- 63
- Citations by year
- 2026: 2 · 2025: 4 · 2024: 2 · 2023: 2 · 2022: 6 · 2021: 7 · 2020: 9 · 2019: 11 · 2018: 9 · 2017: 5 · 2016: 12 · 2015: 8 · 2014: 6 · 2013: 9 · 2012: 11
- FWCI
- 3.51
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- New Phytologist (publishedVersion)
- PubMed (publishedVersion)
- Dépôt institutionnel de l'Université libre de Bruxelles (Université Libre de Bruxelles) (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Micronutrient Interactions and Effects
- Physical Sciences › Environmental Science › Pollution › Heavy metals in environment
- Keywords
- zinc tolerance, Arabidopsis halleri, divergent selection, standing genetic variation, microsatellite markers, metal hyperaccumulation
- MeSH terms
- Adaptation, Biological, Phenotype, Photosynthesis, Polymorphism, Genetic, Selection, Genetic, Zinc, Arabidopsis, Plant Roots, Plant Shoots, Microsatellite Repeats, Photosystem II Protein Complex
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review