Comparative understanding of metal hyperaccumulation in plants: a mini-review
Abstract
Hyperaccumulator plants are ideal models for investigating the regulatory mechanisms of plant metal homeostasis and environmental adaptation due to their notable traits of metal accumulation and tolerance. These traits may benefit either the biofortification of essential mineral nutrients or the phytoremediation of nonessential toxic metals. A common mechanism by which elevated expression of key genes involved in metal transport or chelation contributes to hyperaccumulation and hypertolerance was proposed mainly from studies examining two Brassicaceae hyperaccumulators, namely Arabidopsis halleri and Noccaea caerulescens (formerly Thlaspi caerulescens). Meanwhile, recent findings regarding systems outside the Brassicaceae hyperaccumulators indicated that functional enhancement of key genes might represent a strategy evolved by hyperaccumulator plants. This review provides a brief outline of metal hyperaccumulation in plants and highlights commonalities and differences among various hyperaccumulators.
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Hyperaccumulator plant species have evolved adaptations for hypertolerance and detoxification of metals and metalloids.
“In addition, these plant species have evolved to possess adaptations for hypertolerance and detoxification of metal and metalloids (Angulo-Bejarano et al., 2021; Peng et al., 2021; Rai et al., 2021).”
From Plant hyperaccumulators: a state-of-the-art review on mechanism of heavy metal transport and sequestration (2025) · cites this paper as Peng et al., 2021
Cites
Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting
Rascio, N., & Navari-Izzo, F. (2011) · Plant Science · doi:10.1016/j.plantsci.2010.08.016 · Cited by 2,012 · see citing works
Marra, R. E., Douglas, S. M., & Maier, C. T. (2005) · Cited by 1,816 · see citing works
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
Molecular mechanisms of metal hyperaccumulation in plants
Verbruggen, N., Hermans, C., & Schat, H. (2009) · New Phytologist · doi:10.1111/j.1469-8137.2008.02748.x · Cited by 1,071 · see citing works
Free histidine as a metal chelator in plants that accumulate nickel
Krämer, U., Cotter-Howells, J. D., Charnock, J., Baker, A. J. M., & Smith, J. A. C. (1996) · Nature · doi:10.1038/379635a0 · Cited by 963 · 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
A global database for plants that hyperaccumulate metal and metalloid trace elements
Reeves, R. D., Baker, A. J. M., Jaffré, T., Erskine, P. D., Echevarria, G., & van der Ent, A. (2018) · New Phytologist · doi:10.1111/nph.14907 · Cited by 769 · see citing works
Krzesłowska, M. (2010) · Acta Physiologiae Plantarum · doi:10.1007/s11738-010-0581-z · Cited by 716 · 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
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
Talke, I. N., Hanikenne, M., & Krämer, U. (2006) · Plant Physiology · doi:10.1104/pp.105.076232 · Cited by 452 · see citing works
Krämer, U., Pickering, I. J., Prince, R. C., Raskin, I., & Salt, D. E. (2000) · PLANT PHYSIOLOGY · doi:10.1104/pp.122.4.1343 · Cited by 449 · see citing works
Cellular Compartmentation of Zinc in Leaves of the Hyperaccumulator Thlaspi caerulescens1
Küpper, H., Zhao, F. J., & McGrath, S. P. (1999) · PLANT PHYSIOLOGY · doi:10.1104/pp.119.1.305 · Cited by 444 · 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
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
Subcellular Distribution and Chemical Form of Cadmium in Bean Plants
Weigel, H. J., & Jäger, H. J. (1980) · PLANT PHYSIOLOGY · doi:10.1104/pp.65.3.480 · Cited by 392 · see citing works
Küpper, H., Lombi, E., Zhao, F. J., Wieshammer, G., & McGrath, S. P. (2001) · Journal of Experimental Botany · doi:10.1093/jexbot/52.365.2291 · Cited by 359 · 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
Weber, M., Trampczynska, A., & Clemens, S. (2006) · Plant Cell & Environment · doi:10.1111/j.1365-3040.2005.01479.x · Cited by 329 · 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
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
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
The Role of Free Histidine in Xylem Loading of Nickel inAlyssum lesbiacum and Brassica juncea
Kerkeb, L., & Krämer, U. (2003) · PLANT PHYSIOLOGY · doi:10.1104/pp102.010686 · Cited by 271 · see citing works
A 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
Ueno, D., Milner, M. J., Yamaji, N., Yokosho, K., Koyama, E., Clemencia Zambrano, M., Kaskie, M., Ebbs, S., Kochian, L. V., & Ma, J. F. (2011) · The Plant Journal · doi:10.1111/j.1365-313x.2011.04548.x · Cited by 243 · see citing works
Feng, J. X., Ueno, D., Zhao, F. J., & McGrath, S. P. (2004) · Planta · doi:10.1007/s00425-004-1392-5 · Cited by 237 · see citing works
Elevated Nicotianamine Levels in Arabidopsis halleri Roots Play a Key Role in Zinc Hyperaccumulation
Deinlein, U., Weber, M., Schmidt, H., Rensch, S., Trampczynska, A., Hansen, T. H., Husted, S., Schjoerring, J. K., Talke, I. N., Krämer, U., et al. (2012) · The Plant Cell · doi:10.1105/tpc.111.095000 · Cited by 227 · see citing works
A comparison of the <i>Thlaspi caerulescens</i> and <i>Thlaspi arvense</i> shoot transcriptomes
Hammond, J. P., Bowen, H. C., White, P. J., Mills, V., Pyke, K. A., Baker, A. J. M., Whiting, S. N., May, S. T., & Broadley, M. R. (2006) · New Phytologist · doi:10.1111/j.1469-8137.2006.01662.x · Cited by 223 · see citing works
Gendre, D., Czernic, P., Conéjéro, G., Pianelli, K., Briat, J., Lebrun, M., & Mari, S. (2007) · The Plant Journal · doi:10.1111/j.1365-313x.2006.02937.x · Cited by 221 · see citing works
Gustin, J. L., Loureiro, M. E., Kim, D., Na, G., Tikhonova, M., & Salt, D. E. (2009) · The Plant Journal · doi:10.1111/j.1365-313x.2008.03754.x · Cited by 203 · cited 2× · see citing works
“…thaliana microarray system revealed that genes that control many key steps of metal transport and chelation exhibit increased expression (Becher et al. 2004; Weber et al. 2004, 2005; Chiang et al. 2006; Filatov et al. 2006; Hammond et al. 2006; Talke et al. 2006; van de Mortel et al. 2006).”
BackgroundHoof, 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
Distribution of cadmium in leaves of Thlaspi caerulescens
Cosio, C. (2005) · Journal of Experimental Botany · doi:10.1093/jxb/eri062 · Cited by 191 · see citing works
Cadmium tolerance in Thlaspi caerulescensII. Localization of cadmium in Thlaspi caerulescens
Wójcik, M., Vangronsveld, J., DAHAEN, J., & TUKIENDORF, A. (2005) · Environmental and Experimental Botany · doi:10.1016/s0098-8472(04)00047-4 · Cited by 187 · see citing works
Chiang, H.-C., Lo, J.-C., & Yeh, K.-C. (2006) · Environmental Science & Technology · doi:10.1021/es061432y · Cited by 182 · see citing works
Willems, 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
Kawachi, M., Kobae, Y., Mimura, T., & Maeshima, M. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m707646200 · Cited by 177 · see citing works
Ingle, R. A., Mugford, S. T., Rees, J. D., Campbell, M. M., & Smith, J. A. C. (2005) · The Plant Cell · doi:10.1105/tpc.104.030577 · Cited by 176 · see citing works
Peng, J., Wang, Y. J., Ding, G., Ma, H., Zhang, Y., & Gong, J. (2016) · Molecular Plant · doi:10.1016/j.molp.2016.12.007 · Cited by 175 · see citing works
Self-citationGao, J., Sun, L. V., Yang, X., & Liu, J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0064643 · Cited by 150 · see citing works
Persans, M. W., Yan, X., Patnoe, J.-M. M. L., Krämer, U., & Salt, D. E. (1999) · PLANT PHYSIOLOGY · doi:10.1104/pp.121.4.1117 · Cited by 146 · see citing works
Vacuolar sequestration capacity and long-distance metal transport in plants
Peng, J., & Gong, J. (2014) · Frontiers in Plant Science · doi:10.3389/fpls.2014.00019 · Cited by 136 · see citing works
Self-citationLuo, J., Tao, Q., Jupa, R., Liu, Y., Wu, K., Song, Y., Li, J., Huang, Y., Zou, L., Liang, Y., et al. (2019) · Environmental Science & Technology · doi:10.1021/acs.est.9b01093 · Cited by 135 · see citing works
Wood, J. L., Tang, C., & Franks, A. E. (2016) · Soil Biology and Biochemistry · doi:10.1016/j.soilbio.2016.08.021 · Cited by 128 · see citing works
Meyer, C.-L., Juraniec, M., Huguet, S., Rodriguez, E. C., Salis, P., Isaure, M., Goormaghtigh, E., & Verbruggen, N. (2015) · Journal of Experimental Botany · doi:10.1093/jxb/erv144 · Cited by 126 · 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
Roosens, N. H., Leplae, R., Bernard, C., & Verbruggen, N. (2005) · Planta · doi:10.1007/s00425-005-0006-1 · Cited by 113 · see citing works
Zhao, H., Wang, L., Zhao, F., Wu, L., Liu, A., & Xu, W. (2019) · Plant, Cell & Environment · doi:10.1111/pce.13456 · Cited by 112 · 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
Tsednee, M., Yang, S.-C., Lee, D., & Yeh, K. (2014) · PLANT PHYSIOLOGY · doi:10.1104/pp.114.241224 · Cited by 91 · see citing works
FILATOV, V., DOWDLE, J., SMIRNOFF, N., FORD‐LLOYD, B., NEWBURY, H. J., & MACNAIR, M. R. (2006) · Molecular Ecology · doi:10.1111/j.1365-294x.2006.02981.x · Cited by 82 · see citing works
Peng, J., Ding, G., Meng, S., Yi, H., & Gong, J. (2017) · Plant Cell & Environment · doi:10.1111/pce.12929 · Cited by 80 · see citing works
Self-citationCornu, J., Deinlein, U., Höreth, S., Braun, M., Schmidt, H., Weber, M., Persson, D. P., Husted, S., Schjoerring, J. K., & Clemens, S. (2014) · New Phytologist · doi:10.1111/nph.13237 · Cited by 72 · see citing works
Functional analysis of the threeHMA4copies of the metal hyperaccumulatorArabidopsis halleri
Nouet, C., Charlier, J.-B., Carnol, M., Bosman, B., Farnir, F., Motté, P., & Hanikenne, M. (2015) · Journal of Experimental Botany · doi:10.1093/jxb/erv280 · Cited by 70 · see citing works
SaZIP4, an uptake transporter of Zn/Cd hyperaccumulator Sedum alfredii Hance
Yang, Q., Ma, X.-X., Luo, S., Gao, J., Yang, X., & Feng, Y. (2018) · Environmental and Experimental Botany · doi:10.1016/j.envexpbot.2018.06.021 · Cited by 70 · see citing works
Meier, S., Adams, N., Wolf, M., Balkwill, K., Muasya, A. M., Gehring, C., Bishop, J. M., & Ingle, R. A. (2018) · The Plant Journal · doi:10.1111/tpj.14008 · Cited by 44 · see citing works
Ebbs, S. D., Zambrano, M. C., Spiller, S. M., & Newville, M. G. (2008) · New Phytologist · doi:10.1111/j.1469-8137.2008.02693.x · Cited by 43 · see citing works
Becher, M., Talke, I. N., Krall, L., et al. (2004) · Max Planck Institute for Plasma Physics · Cited by 39 · see citing works
Uraguchi, S., Weber, M., & Clemens, S. (2019) · Plant Cell & Environment · doi:10.1111/pce.13541 · Cited by 25 · see citing works
Liu, H., Zhao, H., Wu, L., et al. (2017) · Frontiers in Plant Science · doi:10.3389/fpls.2017.01047 · Cited by 24 · see citing works
The role of free histidine in xylem loading of nickel in Alyssum lesbiacum and Brassica juncea
Kerkeb, L., & Kramer, U. (2002) · Max Planck Institute for Plasma Physics · Cited by 16 · see citing works
Ma, J. F., Ueno, D., Zhao, F.-J., et al. (2005) · Rothamsted Repository (Rothamsted Repository) · Cited by 10 · see citing works
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Chen, L., Beiyuan, J., Hu, W., Zhang, Z., Duan, C., Cui, Q., Zhu, X., He, H., Huang, X., & Fang, L. (2022) · Chemosphere · doi:10.1016/j.chemosphere.2022.133577 · Cited by 160 · see citing works
Reducing heavy metal contamination in soil and water using phytoremediation
Zhakypbek, Y., Kossalbayev, B. D., Belkozhayev, A. M., Murat, T., Tursbekov, S., Abdalimov, E., Pashkovskiy, P., Kreslavski, V., Kuznetsov, V., & Allakhverdiev, S. I. (2024) · Plants · doi:10.3390/plants13111534 · Cited by 86 · see citing works
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“In addition, these plant species have evolved to possess adaptations for hypertolerance and detoxi fi cation of metal and metalloids (Angulo-Bejarano et al., 2021; Peng et al., 2021; Rai et al., 2021).”
- Authors
- Peng, J.-S., Guan, Y.-H., Lin, X.-J., Xu, X.-J., Xiao, L., Wang, H.-H., & Meng, S.
- Affiliations
- Hunan University of Science and Technology (CN)
- Hunan Agricultural University (CN)
- Corresponding author
- Peng, Jia-Shi
- Meng, Shuan
- Venue
- Environmental Geochemistry and Health
- Published
- 2020-02-14
- Volume
- 43
- Issue
- 4
- Pages
- 1599-1607
- ISSN
- 0269-4042 (ISSN-L)
- 1573-2983
- OpenAlex
- W3005630919
- Cited by
- 63
- References
- 61
- Citations by year
- 2026: 7 · 2025: 10 · 2024: 11 · 2023: 8 · 2022: 11 · 2021: 12 · 2020: 4
- FWCI
- 0.39
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Environmental Geochemistry and Health (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Natural Science Foundation of China (31700212)
- Topics
- Physical Sciences › Environmental Science › Pollution › Heavy metals in environment
- Physical Sciences › Chemistry › Analytical Chemistry › Heavy Metals in Plants
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Micronutrient Interactions and Effects
- Keywords
- metal hyperaccumulation, hyperaccumulator plants, plant metal homeostasis, metal tolerance, phytoremediation, biofortification, metal transport genes, metal chelation, Arabidopsis halleri, Noccaea caerulescens, Brassicaceae
- MeSH terms
- Biodegradation, Environmental, Metals, Plants
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