A broad-scale analysis of population differentiation for Zn tolerance in an emerging model species for tolerance study: Arabidopsis halleri (Brassicaceae)
Abstract
Although current knowledge about the overall distribution of zinc (Zn) tolerance in Arabidopsis halleri populations is scarce, the species is an emerging model for the study of heavy metal tolerance in plants. We attempted to improve this knowledge by testing the Zn tolerance of scattered European metallicolous (M) and nonmetallicolous (NM) populations of A. h. subsp. halleri and A. h. subsp. ovirensis in hydroponic culture. The occurrence of constitutive tolerance was unconditionally established in A. h. halleri and tolerance was extended to the subspecies ovirensis. M populations were the most tolerant but there was a continuous range of variation in tolerance from NM to M populations. Finally, relatively high levels of tolerance were detected in some NM populations, suggesting that enhanced tolerance could be present at high frequency in populations that have not experienced metal exposure. We used our results to argue the evolutionary dynamics and origin of Zn tolerance in A. halleri.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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 Pauwels et al., 2006
The Discussion ('Constitutive zinc tolerance in the A. halleri population in Europe'; page unavailable) reports high Zn tolerance across the populations tested, and 'Evolution of Zn tolerance in Europe' reports significant differences among populations. The Introduction describes A. halleri as tolerating Zn and Cd, but the paper does not establish species-wide Cd tolerance or significant variation in Cd tolerance among populations. (LLM, conf=0.88)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Endless Forms: Species and Speciation
Howard, D. J., & Berlocher, S. H. (1998) · Medical Entomology and Zoology · Cited by 2,516 · 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 in Plants: Evolutionary Aspects
Shaw, A. J. (1989) · Cited by 1,154 · see citing works
Plants that Hyperaccumulate Heavy Metals
(1998) · CABI eBooks · doi:10.1079/9780851992365.0000 · Cited by 1,031 · see citing works
Heavy metal tolerance of plants
Bothe, H. (2014) · Acta Biologica Cracoviensia. Series Zoologia · Cited by 1,008 · see citing works
Heavy Metal Tolerance in Plants
Antonovics, J., Bradshaw, A. D., & Turner, R. G. (1971) · Advances in ecological research/Advances in Ecological Research · doi:10.1016/s0065-2504(08)60202-0 · Cited by 858 · see citing works
Becher, M., Talke, I. N., Krall, L., & Krämer, U. (2004) · The Plant Journal · doi:10.1046/j.1365-313x.2003.01959.x · Cited by 568 · see citing works
Serpentine and its vegetation: A multidisciplinary approach
(1989) · Quaternary Research · doi:10.1016/0033-5894(89)90112-9 · Cited by 535 · see citing works
Strategies of heavy metal uptake by three plant species growing near a metal smelter
Dahmani-Muller, H., van Oort, F., Gélie, B., & Balabane, M. (2000) · Environmental Pollution · doi:10.1016/s0269-7491(99)00262-6 · Cited by 493 · see citing works
Weber, M., Harada, E., Vess, C., Roepenack‐Lahaye, E. V., & Clemens, S. (2004) · The Plant Journal · doi:10.1046/j.1365-313x.2003.01960.x · Cited by 440 · see citing works
The Genetic Basis of Metal Hyperaccumulation in Plants
Pollard, A. J., Dandridge, K. L., Harper, F. A., & Smith, J. A. C. (2002) · Critical Reviews in Plant Sciences · doi:10.1080/0735-260291044359 · Cited by 424 · see citing works
Koch, М. A., Haubold, B., & Mitchell‐Olds, T. (2001) · American Journal of Botany · doi:10.2307/2657117 · Cited by 401 · see citing works
Evolutionary and ecological functional genomics
Feder, M. E., & Mitchell‐Olds, T. (2003) · Nature Reviews Genetics · doi:10.1038/nrg1128 · Cited by 384 · see citing works
The Origin, Expansion, and Demise of Plant Species
Levin, D. A. (2000) · doi:10.1093/oso/9780195127287.001.0001 · Cited by 364 · see citing works
Assunção, A. G. L., Schat, H., & Aarts, M. G. M. (2003) · New Phytologist · doi:10.1046/j.1469-8137.2003.00820.x · Cited by 358 · see citing works
The genetics of metal tolerance in vascular plants
Macnair, M. R. (1993) · New Phytologist · doi:10.1111/j.1469-8137.1993.tb03846.x · Cited by 322 · see citing works
Arabidopsis thaliana and its wild relatives: a model system for ecology and evolution
Mitchell‐Olds, T. (2001) · Trends in Ecology & Evolution · doi:10.1016/s0169-5347(01)02291-1 · Cited by 303 · see citing works
Dräger, D. B., Desbrosses‐Fonrouge, A., Krach, C., Chardonnens, A. N., Meyer, R. C., Saumitou‐Laprade, P., & Krämer, U. (2004) · The Plant Journal · doi:10.1111/j.1365-313x.2004.02143.x · Cited by 294 · see citing works
Self-citationThe 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-citationThe 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 · cited 4× · see citing works
“…(Koch et al., 1998; Assunção et al., 2003b), this knowledge remains sparse in A. halleri which was sometimes said to be typically found on metalliferous soils (Dahmani-Muller et al., 2000; Pollard et al., 2002) although numerous NM populations have been mentioned (Bert et al., 2000, 2002).”
BackgroundResultInfluentialSelf-citationAn Essay: The Stimulus of Unusual Geologies for Plant Speciation
Kruckeberg, A. R. (1986) · Systematic Botany · doi:10.2307/2419082 · Cited by 209 · see citing works
Genetic basis of Cd tolerance and hyperaccumulation in Arabidopsis halleri
Bert, V., Meerts, P., Saumitou‐Laprade, P., Salis, P., Grüber, W., & Verbruggen, N. (2003) · Plant and Soil · doi:10.1023/a:1022580325301 · Cited by 208 · see citing works
Self-citationHoof, N. A. L. M. V., Hassinen, V. H., Hakvoort, H. W. J., Ballintijn, K. F., Schat, H., Verkleij, J. A. C., Ernst, W. H. O., Kärenlampi, S. O., & Tervahauta, A. I. (2001) · PLANT PHYSIOLOGY · doi:10.1104/pp.126.4.1519 · Cited by 201 · see citing works
Genetic 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-citationSerpentine and Its Vegetation: A Multidisciplinary Approach.
Ware, S. A., & Brooks, R. R. (1988) · Bulletin of the Torrey Botanical Club · doi:10.2307/2996568 · Cited by 185 · see citing works
Differentiation of Allelic Frequencies at Quantitative Trait Loci Affecting Locally Adaptive Traits
Latta, R. G. (1998) · The American Naturalist · doi:10.1086/286119 · Cited by 182 · 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
Vekemans, X., & Lefebvre, C. (1997) · Journal of Evolutionary Biology · doi:10.1046/j.1420-9101.1997.10020175.x · Cited by 120 · see citing works
Plants and the chemical elements: Biochemistry, uptake, tolerance and toxicity
Lepp, N. W. (1995) · Environmental Pollution · doi:10.1016/0269-7491(95)90037-3 · Cited by 114 · see citing works
Palatability of Thlaspi caerulescens for snails: influence of zinc and glucosinolates
Noret, N., Meerts, P., Tolrà, R. P., Poschenrieder, C., Barceló, J. A., & Escarré, J. (2004) · New Phytologist · doi:10.1111/j.1469-8137.2004.01286.x · Cited by 90 · see citing works
The 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
Linking molecular insight and ecological research
Jackson, R. B., Linder, C. R., Lynch, M., Purugganan, M. D., Somerville, S. C., & Thayer, S. S. (2002) · Trends in Ecology & Evolution · doi:10.1016/s0169-5347(02)02571-5 · Cited by 88 · see citing works
Adaptation to environmental stress: a rare or frequent driver of speciation?
Lexer, C., & Fay, M. F. (2005) · Journal of Evolutionary Biology · doi:10.1111/j.1420-9101.2005.00901.x · Cited by 88 · see citing works
Ernst, W. H. O. (2024) · CRC Press eBooks · doi:10.1201/9781003574903-4 · Cited by 87 · 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
Assunção, 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.1469-8137.2003.00758.x · 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
Schat, H., Vooijs, R., & Kuiper, E. (1996) · Evolution · doi:10.2307/2410747 · Cited by 78 · see citing works
THE EFFECT OF SERPENTINE ON THE POPULATION STRUCTURE OF SILENE DIOICA (CARYOPHYLLACEAE)
Westerbergh, A., & Saura, A. (1992) · Evolution · doi:10.1111/j.1558-5646.1992.tb01143.x · Cited by 74 · 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-citationWhere is the cost in copper tolerance in Mimulus guttatus? Testing the trade‐off hypothesis
Harper, F. A., SMITH, S. E., & Macnair, M. R. (1997) · Functional Ecology · doi:10.1046/j.1365-2435.1997.00155.x · Cited by 67 · see citing works
THLASPI CAERULESCENS J. & C. PRESL. (T. ALPESTRE L.) IN BRITAIN
Ingrouille, M., & Smirnoff, N. (1986) · New Phytologist · doi:10.1111/j.1469-8137.1986.tb00812.x · Cited by 60 · 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
Harper, F. A., SMITH, S. E., & Macnair, M. R. (1997) · New Phytologist · doi:10.1046/j.1469-8137.1997.00761.x · Cited by 50 · see citing works
Serpentine and non-serpentine Silene dioica plants do not differ in nickel tolerance
Westerbergh, A. (1994) · Plant and Soil · doi:10.1007/bf00007956 · Cited by 39 · see citing works
Frérot, H., Lefèbvre, C., Petit, C., Collin, C., dos Santos, A., & Escarré, J. (2004) · New Phytologist · doi:10.1111/j.1469-8137.2004.01227.x · Cited by 38 · see citing works
Self-citationEndemic metallophytes: their taxonomic, genetic, and evolutionary attributes.
Kruckeberg, A. R., Kruckeberg, A. L., & Shaw, A. J. (1990) · Cited by 31 · see citing works
Harper, F. A., SMITH, S. E., & Macnair, M. R. (1998) · New Phytologist · doi:10.1046/j.1469-8137.1998.00312.x · Cited by 28 · see citing works
7. S. Prát: Die Erblichkeit der Resistenz gegen Kupfer
(1934) · Berichte der Deutschen Botanischen Gesellschaft · doi:10.1111/j.1438-8677.1934.tb01655.x · Cited by 27 · see citing works
The Effect of Serpentine on the Population Structure of Silene dioica (Caryophyllaceae)
Westerbergh, A., & Saura, A. (1992) · Evolution · doi:10.2307/2409956 · Cited by 24 · see citing works
Heavy metal tolerance of Cardaminopsis halleri (L.) Hayek populations in the Polish Tatra Mts.
Fabiszewski, J. (2014) · Acta Societatis Botanicorum Poloniae · doi:10.5586/asbp.1986.037 · Cited by 9 · see citing works
Berton, A. (1946) · Bulletin de la Société Botanique de France · doi:10.1080/00378941.1946.10834513 · Cited by 9 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Metal hyperaccumulation in plants
Krämer, U. (2010) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-042809-112156 · Cited by 1,284 · see citing works
Rieseberg, L. H., & Blackman, B. K. (2010) · Annals of Botany · doi:10.1093/aob/mcq126 · Cited by 341 · 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-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-citationCd 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
Shahzad, Z., Gosti, F., Frérot, H., Lacombe, E., Roosens, N., Saumitou-Laprade, P., & Berthomieu, P. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1000911 · Cited by 124 · see citing works
Self-citationMeyer, C., Kostecka, A. A., Saumitou‐Laprade, P., Créach, A., Castric, V., Pauwels, M., & Frérot, H. (2010) · New Phytologist · doi:10.1111/j.1469-8137.2009.03062.x · Cited by 110 · see citing works
Self-citationFrérot, 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
- Pauwels, M., Frérot, H., Bonnin, I., & Saumitou-laprade, P.
- Affiliations
- Université de Lille (FR)
- Centre National de la Recherche Scientifique (FR)
- Laboratoire de Génétique et Evolution des Populations Végétales, Université des Sciences et Technologies de Lille, Villeneuve d'Ascq Cedex, France
- Corresponding author
- Pauwels, Maxime
- Venue
- Journal of Evolutionary Biology
- Publisher
- Oxford University Press (OUP)
- Published
- 2006-11-01
- Volume
- 19
- Issue
- 6
- Pages
- 1838-1850
- ISSN
- 1010-061X (ISSN-L)
- 1420-9101
- OpenAlex
- W2003002334
- Cited by
- 104
- References
- 61
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 1 · 2023: 3 · 2022: 6 · 2021: 1 · 2020: 6 · 2019: 6 · 2018: 6 · 2017: 6 · 2016: 11 · 2015: 6 · 2014: 3 · 2013: 3 · 2012: 8
- FWCI
- 5.70
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- Locations
- Journal of Evolutionary Biology (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Topics
- Physical Sciences › Environmental Science › Pollution › Heavy metals in environment
- 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
- Keywords
- Arabidopsis halleri, zinc tolerance, heavy metal tolerance, genetic differentiation, Brassicaceae, hydroponics
- MeSH terms
- Drug Tolerance, Ecology, Europe, Genetics, Population, Soil Pollutants, Zinc, Arabidopsis
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