The five AhMTP1 zinc transporters undergo different evolutionary fates towards adaptive evolution to zinc tolerance in Arabidopsis halleri
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Gene duplication is a major mechanism facilitating adaptation to changing environments. From recent genomic analyses, the acquisition of zinc hypertolerance and hyperaccumulation characters discriminating Arabidopsis halleri from its zinc sensitive/non-accumulator closest relatives Arabidopsis lyrata and Arabidopsis thaliana was proposed to rely on duplication of genes controlling zinc transport or zinc tolerance. Metal Tolerance Protein 1 (MTP1) is one of these genes. It encodes a Zn(2+)/H(+) antiporter involved in cytoplasmic zinc detoxification and thus in zinc tolerance. MTP1 was proposed to be triplicated in A. halleri, while it is present in single copy in A. thaliana and A. lyrata. Two of the three AhMTP1 paralogues were shown to co-segregate with zinc tolerance in a BC1 progeny from a cross between A. halleri and A. lyrata. In this work, the MTP1 family was characterized at both the genomic and functional levels in A. halleri. Five MTP1 paralogues were found to be present in A. halleri, AhMTP1-A1, -A2, -B, -C, and -D. Interestingly, one of the two newly identified AhMTP1 paralogues was not fixed at least in one A. halleri population. All MTP1s were expressed, but transcript accumulation of the paralogues co-segregating with zinc tolerance in the A. halleri X A. lyrata BC1 progeny was markedly higher than that of the other paralogues. All MTP1s displayed the ability to functionally complement a Saccharomyces cerevisiae zinc hypersensitive mutant. However, the paralogue showing the least complementation of the yeast mutant phenotype was one of the paralogues co-segregating with zinc tolerance. From our results, the hypothesis that pentaplication of MTP1 could be a major basis of the zinc tolerance character in A. halleri is strongly counter-balanced by the fact that members of the MTP1 family are likely to experience different evolutionary fates, some of which not concurring to increase zinc tolerance.
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Comparative expression analysis reported that later genomic evolution was displayed by the enhanced copy number of transporters such as HMA4 to 3 and MTP1 to 5 in Arabidopsis halleri compared to single-copy found in wild-type A. thaliana.
“A comparative expression analysis reported that later genomic evolution was displayed by the enhanced copy number of transporters such as; HMA4 to 3 and MTP1 to 5 in Arabidopsis halleri compared to single-copy found in wild-type A. thaliana (Hanikenne et al., 2008; Shahzad et al., 2010).”
From Plant hyperaccumulators: a state-of-the-art review on mechanism of heavy metal transport and sequestration (2025) · cites this paper as Shahzad et al., 2010
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Cites
Krogh, A., Larsson, B., von Heijne, G., & Sonnhammer, E. L. L. (2001) · Journal of Molecular Biology · doi:10.1006/jmbi.2000.4315 · Cited by 12,654 · see citing works
Church, G. M., & Gilbert, W. (1984) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.81.7.1991 · Cited by 8,213 · see citing works
Ohno, S. (1970) · doi:10.1007/978-3-642-86659-3 · Cited by 7,833 · see citing works
THE ESTIMATION OF MAP DISTANCES FROM RECOMBINATION VALUES
Kosambi, D. D. (1943) · Annals of Eugenics · doi:10.1111/j.1469-1809.1943.tb02321.x · Cited by 5,852 · see citing works
Preservation of Duplicate Genes by Complementary, Degenerative Mutations
Force, A., Lynch, M., Pickett, F. B., Amores, A., Yan, Y.-L., & Postlethwait, J. (1999) · Genetics · doi:10.1093/genetics/151.4.1531 · Cited by 3,529 · see citing works
Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method
Gietz, R. D., & Woods, R. A. (2002) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(02)50957-5 · Cited by 2,890 · see citing works
Evolution by gene duplication: An update
Zhang, J. (2003) · Trends in Ecology & Evolution · doi:10.1016/s0169-5347(03)00033-8 · Cited by 2,201 · see citing works
Pilon‐Smits, E. A. H. (2005) · Annual Review of Plant Biology · doi:10.1146/annurev.arplant.56.032604.144214 · Cited by 2,085 · see citing works
The Physcomitrella Genome Reveals Evolutionary Insights into the Conquest of Land by Plants
Rensing, S. A., Lang, D., Zimmer, A. D., Terry, A. Y., Salamov, A. A., Shapiro, H., Nishiyama, T., Perroud, P., Lindquist, E., Kamisugi, Y., et al. (2007) · Science · doi:10.1126/science.1150646 · Cited by 1,856 · see citing works
The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus)
Ming, R., Hou, S., Feng, Y., Yu, Q., Dionne‐Laporte, A., Saw, J. H. W., Senin, P., Wang, W., Ly, B. V., Lewis, K. L. T., et al. (2008) · Nature · doi:10.1038/nature06856 · Cited by 1,087 · see citing works
A High Quality Draft Consensus Sequence of the Genome of a Heterozygous Grapevine Variety
Velasco, R., Zharkikh, A., Troggio, M., Cartwright, D., Cestaro, A., Pruss, D., Pindo, M., Fitzgerald, L. M., Vezzulli, S., Reid, J., et al. (2007) · PLoS ONE · doi:10.1371/journal.pone.0001326 · Cited by 1,046 · see citing works
Heavy metal tolerance of plants
Bothe, H. (2014) · Acta Biologica Cracoviensia. Series Zoologia · Cited by 1,008 · see citing works
Gene duplication and evolutionary novelty in plants
Flagel, L. E., & Wendel, J. F. (2009) · New Phytologist · doi:10.1111/j.1469-8137.2009.02923.x · Cited by 969 · 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
Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4
Hanikenne, M., Talke, I. N., Haydon, M. J., Lanz, C., Nolte, A., Motte, P., Kroymann, J., Weigel, D., & Krämer, U. (2008) · Nature · doi:10.1038/nature06877 · Cited by 812 · see citing works
The ABC’s of comparative genomics in the Brassicaceae: building blocks of crucifer genomes
Schranz, M. E., Lysak, M. A., & Mitchell-Olds, T. (2006) · Trends in Plant Science · doi:10.1016/j.tplants.2006.09.002 · Cited by 575 · see citing works
Talke, I. N., Hanikenne, M., & Krämer, U. (2006) · Plant Physiology · doi:10.1104/pp.105.076232 · Cited by 452 · see citing works
van der Zaal, B. J., Neuteboom, L. W., Pinas, J. E., Chardonnens, A. N., Schat, H., Verkleij, J. A. C., & Hooykaas, P. J. J. (1999) · PLANT PHYSIOLOGY · doi:10.1104/pp.119.3.1047 · Cited by 415 · see citing works
Zinc transporters that regulate vacuolar zinc storage in Saccharomyces cerevisiae
MacDiarmid, C. W., Gaither, L. A., & Eide, D. (2000) · The EMBO Journal · doi:10.1093/emboj/19.12.2845 · Cited by 389 · see citing works
Gene Duplication: The Genomic Trade in Spare Parts
Hurles, M. E. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020206 · Cited by 359 · see citing works
Persans, M. W., Nieman, K., & Salt, D. E. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.171039798 · Cited by 317 · see citing works
Desbrosses-Fonrouge, A.-G., Voigt, K., Schröder, A., Arrivault, S., Thomine, S., & Krämer, U. (2005) · FEBS Letters · doi:10.1016/j.febslet.2005.06.046 · Cited by 305 · 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-citationArabidopsis IRT3 is a zinc‐regulated and plasma membrane localized zinc/iron transporter
Lin, Y., Liang, H., Yang, S., Boch, A., Clemens, S., Chen, C., Wu, J.-F., Huang, J., & Yeh, K. (2009) · New Phytologist · doi:10.1111/j.1469-8137.2009.02766.x · Cited by 292 · 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-citationMirouze, M., Sels, J., Richard, O., Czernic, P., Loubet, S., Jacquier, A., François, I., Cammue, B. P. A., Lebrun, M., Berthomieu, P., et al. (2006) · The Plant Journal · doi:10.1111/j.1365-313x.2006.02788.x · Cited by 209 · 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-citationKawachi, M., Kobae, Y., Mimura, T., & Maeshima, M. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m707646200 · Cited by 177 · see citing works
Evolution and genetic differentiation among relatives of Arabidopsis thaliana
Koch, М. A., & Matschinger, M. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0701338104 · Cited by 123 · see citing works
Koizumi, S., Suzuki, K., Ogra, Y., et al. (1999) · European Journal of Biochemistry · doi:10.1046/j.1432-1327.1999.00069.x · Cited by 119 · 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-citationPauwels, M., WILLEMS, G., Roosens, N. H. C., Frérot, H., & Saumitou‐Laprade, P. (2007) · Molecular Ecology · doi:10.1111/j.1365-294x.2007.03486.x · Cited by 49 · see citing works
Self-citationRoosens, 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-citationLacombe, E., Cossegal, M., Mirouze, M., Adam, T., Varoquaux, F., Loubet, S., Piffanelli, P., Lebrun, M., & Berthomieu, P. (2008) · Plant Science · doi:10.1016/j.plantsci.2008.03.020 · Cited by 7 · see citing works
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Balafrej, H., Bogusz, D., Triqui, Z.-E. A., Guedira, A., Bendaou, N., Smouni, A., & Fahr, M. (2020) · Plants · doi:10.3390/plants9050562 · Cited by 275 · see citing works
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Manara, A., Fasani, E., Furini, A., & DalCorso, G. (2020) · Plant, Cell & Environment · doi:10.1111/pce.13821 · Cited by 124 · see citing works
Isaure, M.-P., Huguet, S., Meyer, C.-L., Castillo-Michel, H., Testemale, D., Vantelon, D., Saumitou-Laprade, P., Verbruggen, N., & Sarret, G. (2015) · Journal of Experimental Botany · doi:10.1093/jxb/erv131 · Cited by 96 · see citing works
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Peng, J.-S., Guan, Y.-H., Lin, X.-J., Xu, X.-J., Xiao, L., Wang, H.-H., & Meng, S. (2021) · Environmental Geochemistry and Health · doi:10.1007/s10653-020-00533-2 · Cited by 63 · see citing works
Fukuda, N., Kitajima, N., Terada, Y., Abe, T., Nakai, I., & Hokura, A. (2020) · Metallomics · doi:10.1039/c9mt00243j · Cited by 27 · see citing works
- Authors
- Shahzad, Z., Gosti, F., Frérot, H., Lacombe, E., Roosens, N., Saumitou-Laprade, P., & Berthomieu, P.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Corresponding author
- Berthomieu, Pierre
- Venue
- PLoS Genetics
- Publisher
- Public Library of Science (PLoS)
- Published
- 2010-04-15
- Volume
- 6
- Issue
- 4
- Pages
- e1000911
- ISSN
- 1553-7390 (ISSN-L)
- 1553-7404
- PMC
- PMC2855318
- OpenAlex
- W2000981840
- Cited by
- 124
- References
- 34
- Citations by year
- 2026: 2 · 2025: 4 · 2024: 6 · 2023: 4 · 2022: 2 · 2021: 11 · 2020: 19 · 2019: 5 · 2018: 4 · 2017: 8 · 2016: 10 · 2015: 8 · 2014: 8 · 2013: 13 · 2012: 7
- FWCI
- 12.67
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Genetics (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- HAL (submittedVersion, other-oa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
- Higher Education Commission, Pakistan
- Centre National de la Recherche Scientifique
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Micronutrient Interactions and Effects
- Health Sciences › Nursing › Nutrition and Dietetics › Trace Elements in Health
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
- Keywords
- Arabidopsis halleri, zinc tolerance, zinc hyperaccumulation, zinc transporters, gene duplication, paralogs, adaptive evolution, zinc detoxification, functional complementation, Arabidopsis lyrata, Arabidopsis thaliana
- MeSH terms
- Carrier Proteins, Genetics, Population, Phylogeny, Linkage Disequilibrium, Gene Expression Regulation, Plant, Genome, Plant, Evolution, Molecular, Cation Transport Proteins, Arabidopsis Proteins
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