Abstract
Metals (trace elements) are essential for plants but become toxic at high concentration. Remarkably, about 700 species worldwide are able to accumulate large quantities of metals in their leaves and are therefore called metal hyperaccumulators. In the context of sustainable development, there is renewed interest in understanding the mechanisms of metal hyperaccumulation that may become instrumental for improved metal phytoextraction from contaminated soils and for making metals available at lower environmental cost. In addition, studying the molecular mechanisms of hyperaccumulation in diverse plant species is necessary in order to understand the evolution of this extreme and complex adaptation trait in plants. Our current knowledge of metal hyperaccumulation is based mostly on the analysis of few species from the Brassicaceae family and suggests that the underlying mechanisms result from an exaggeration of the basic mechanisms involved in metal homeostasis. However, the development of Next Generation Sequencing technologies enables the study of new hyperaccumulator species and therefore the revealing of greater diversity in these mechanisms. The goal of this chapter is to provide background information on metal hyperaccumulation and give an instantaneous picture of what is currently known about the molecular mechanisms involved in this trait. We also attempt to outline for the reader the future scientific challenges that this field of research is facing.
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References
Aboudrar W, Schwartz C, Morel JL, Boularbah A (2012) Effect of nickel-resistant rhizosphere bacteria on the uptake of nickel by the hyperaccumulator Noccaea caerulescens under controlled conditions. J Soils Sediment 13:501–507
Ahmadi H, Corso M, Weber M et al (2018) CAX1 suppresses Cd-induced generation of reactive oxygen species in Arabidopsis halleri. Plant Cell Environ 41:2435–2448
Alvarez-Fernandez A, Diaz-Benito P, Abadia A et al (2014) Metal species involved in long distance metal transport in plants. Front Plant Sci 5:105
Alves S, Nabais C, Simoes Goncalves MDL, Dos Santos MMC (2011) Nickel speciation in the xylem sap of the hyperaccumulator Alyssum serpyllifolium ssp. lusitanicum growing on serpentine soils of northeast Portugal. J Plant Physiol 168:1715–1722
Assunção AGL, Bookum WM, Nelissen HJM et al (2003) Differential metal-specific tolerance and accumulation patterns among Thlaspi caerulescens populations originating from different soil types. New Phytol 159:411–419
Assunção AGL, Herrero E, Lin YF et al (2010) Arabidopsis thaliana transcription factors bZIP19 and bZIP23 regulate the adaptation to zinc deficiency. Proc Natl Acad Sci USA 107:10296–10301
Babst-Kostecka A, Schat H, Saumitou-Laprade P et al (2018) Evolutionary dynamics of quantitative variation in an adaptive trait at the regional scale: the case of zinc hyperaccumulation in Arabidopsis halleri. Mol Ecol 27:3257–3273
Baliardini C, Corso M, Verbruggen N (2016) Transcriptomic analysis supports the role of CATION EXCHANGER 1 in cellular homeostasis and oxidative stress limitation during cadmium stress. Plant Signal Behav 11:e1183861
Baliardini C, Meyer C-L, Salis P et al (2015) CATION EXCHANGER1 cosegregates with cadmium tolerance in the metal hyperaccumulator Arabidopsis halleri and plays a role in limiting oxidative stress in Arabidopsis spp. Plant Physiol 169:549–559
Barabasz A, Krämer U, Hanikenne M et al (2010) Metal accumulation in tobacco expressing Arabidopsis halleri metal hyperaccumulation gene depends on external supply. J Exp Bot 61:3057–3067
Barberon M, Berthomieu P, Clairotte M et al (2008) Unequal functional redundancy between the two Arabidopsis thaliana high-affinity sulphate transporters SULTR1;1 and SULTR1;2. New Phytol 180:608–619
Barberon M, Zelazny E, Robert S et al (2011) Monoubiquitin-dependent endocytosis of the Iron-Regulated Transporter 1 (IRT1) transporter controls iron uptake in plants. Proc Natl Acad Sci USA 108:E450–E458
Barillas JRV, Quinn CF, Pilon-Smits EAH (2011) Selenium accumulation in plants-phytotechnological applications and ecological implications. Int J Phytoremediation 13:166–178
Bayçu G, Gevrek-Kürüm N, Moustaka J et al (2017) Cadmium-zinc accumulation and photosystem II responses of Noccaea caerulescens to Cd and Zn exposure. Environ Sci Pollut Res 24:2840–2850
Becher M, Talke IN, Krall L, Krämer U (2004) Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri. Plant J 37:251–268
Bernard C, Roosens N, Czernic P et al (2004) A novel CPx-ATPase from the cadmium hyperaccumulator Thlaspi caerulescens. FEBS Lett 569:140–148
Bert V, Bonnin I, Saumitou-Laprade P et al (2002) Do Arabidopsis halleri from non metallicolous populations accumulate zinc and cadmium more effectively than those from metallicolous populations? New Phytol 155:47–57
Bert V, Macnair MR, De Laguérie P et al (2000) Zinc tolerance and accumualtion in metallicolous and non metallicolous populations of Arabidopsis halleri (Brassicaceae). New Phytol 146:225–233
Besnard G, Basic N, Christin PA et al (2009) Thlaspi caerulescens (Brassicaceae) population genetics in western Switzerland: is the genetic structure affected by natural variation of soil heavy metal concentrations? New Phytol 181:974–984
Boyd R, Martens S (1992) In: The vegetation of ultramafic (serpentine) soils. Baker AJM, Proctor J, Reeves RD (eds) Andover, Hampshire: Intercept Limited, UK, pp 279–289
Boyd RS, Shaw JJ, Martens SN (1994) Nickel hyperaccumulation defends Streptanthus polygaloides (Brassicaceae) against pathogens. Am J Bot 81:294–300
Burkhead JL, Reynolds KA, Abdel-Ghany SE et al (2009) Copper homeostasis. New Phytol 182:799–816
Cabannes E, Buchner P, Broadley MR, Hawkesford MJ (2011) A comparison of sulfate and selenium accumulation in relation to the expression of sulfate transporter genes in Astragalus species. Plant Physiol 157:2227–2239
Cabello-Conejo MI, Becerra-Castro C, Prieto-Fernández A et al (2014) Rhizobacterial inoculants can improve nickel phytoextraction by the hyperaccumulator Alyssum pintodasilvae. Plant Soil 379:35–50
Cabot C, Martos S, Llugany M et al (2019) A role for zinc in plant defense against pathogens and herbivores. Front Plant Sci 10:1171
Cailliatte R, Schikora A, Briat JF et al (2010) High-affinity manganese uptake by the metal transporter NRAMP1 is essential for Arabidopsis growth in low manganese conditions. Plant Cell 22:904–917
Callahan DL, Baker AJM, Kolev SD, Wedd AG (2006) Metal ion ligands in hyperaccumulating plants. J Biol Inorg Chem 11:2–12
Callahan DL, Hare DJ, Bishop DP et al (2016) Elemental imaging of leaves from the metal hyperaccumulating plant Noccaea caerulescens shows different spatial distribution of Ni, Zn and Cd. RSC Adv 6:2337–2344
Callahan DL, Kolev SD, O’Hair RAJ et al (2007) Relationships of nicotianamine and other amino acids with nickel, zinc and iron in Thlaspi hyperaccumulators. New Phytol 176:836–848
Callahan DL, Roessner U, Dumontet V, de Livera AM, Doronila A, Baker AJM, Kolev S (2012) Elemental and metabolite profiling of nickel hyperaccumulators from New Caledonia. Phytochemistry 81:80–89
Camilios-Neto D, Bonato P, Wassem R et al (2014) Dual RNA-seq transcriptional analysis of wheat roots colonized by Azospirillum brasilense reveals up-regulation of nutrient acquisition and cell cycle genes. BMC Genom 15:378
Cao D, Zhang H, Wang Y, Zheng L (2014) Accumulation and distribution characteristics of zinc and cadmium in the hyperaccumulator plant Sedum plumbizincicola. Bull Env Contam Toxicol 93:171–176
Cao X, Luo J, Wang X et al (2020) Responses of soil bacterial community and Cd phytoextraction to a Sedum alfredii—oilseed rape (Brassica napus L. and Brassica juncea L.) intercropping system. Sci Total Environ 723:138152
Cappa JJ, Pilon-Smits EAH (2014) Evolutionary aspects of elemental hyperaccumulation. Planta 239:267–275
Centofanti T, Sayers Z, Cabello-Conejo MI et al (2013) Xylem exudate composition and root-to-shoot nickel translocation in Alyssum species. Plant Soil 373:59–75
Charlier JB, Polese C, Nouet C et al (2015) Zinc triggers a complex transcriptional and post-transcriptional regulation of the metal homeostasis gene FRD3 in Arabidopsis relatives. J Exp Bot 66:3865–3878
Chen K, Wang Y, Zhang R et al (2019) CRISPR/Cas genome editing and precision plant breeding in agriculture. Annu Rev Plant Biol 70:667–697
Chen L, Luo S, Chen J et al (2014) A comparative analysis of endophytic bacterial communities associated with hyperaccumulators growing in mine soils. Env Sci Pollut Res Int 21:7538–7547
Chiang HC, Lo JC, Yeh KC (2006) Genes associated with heavy metal tolerance and accumulation in Zn/Cd hyperaccumulator Arabidopsis halleri: a genomic survey with cDNA microarray. Env Sci Technol 40:6792–6798
Claus J, Bohmann A, Chavarría-Krauser A (2013) Zinc uptake and radial transport in roots of Arabidopsis thaliana: a modelling approach to understand accumulation. Ann Bot 112:369–380
Clauss MJ, Koch MA (2006) Poorly known relatives of Arabidopsis thaliana. Trends Plant Sci 11:449–459
Clemens S (2019) Metal ligands in micronutrient acquisition and homeostasis. Plant Cell Environ 42:2902–2912
Clemens S, Deinlein U, Ahmadi H et al (2013) Nicotianamine is a major player in plant Zn homeostasis. Biometals 26:623–632
Clemens S, Palmgren MG, Krämer U (2002) A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci 7:309–15
Conn SJ, Gilliham M, Athman A et al (2011) Cell-specific vacuolar calcium storage mediated by CAX1 regulates apoplastic calcium concentration, gas exchange, and plant productivity in Arabidopsis. Plant Cell 23:240–257
Conte SS, Walker EL (2012) Genetic and biochemical approaches for studying the Yellow Stripe-Like transporter family in plants. Curr Top Membr 69:295–322
Cornu J, Deinlein U, Horeth S et al (2015) Contrasting effects of nicotianamine synthase knockdown on zinc and nickel tolerance and accumulation in the zinc/cadmium hyperaccumulator Arabidopsis halleri. New Phytol 206:738–750
Corso M, Schvartzman MS, Guzzo F et al (2018) Contrasting cadmium resistance strategies in two metallicolous populations of Arabidopsis halleri. New Phytol 218:283–297
Cosio C, DeSantis L, Frey B et al (2005) Distribution of cadmium in leaves of Thlaspi caerulescens. J Exp Bot 56:765–775
Courbot M, Willems G, Motte P et al (2007) A major QTL for Cd tolerance in Arabidopsis halleri co-localizes with HMA4, a gene encoding a Heavy Metal ATPase. Plant Physiol 144:1052–1065
Craciun AR, Courbot M, Bourgis F et al (2006) Comparative cDNA-AFLP analysis of Cd-tolerant and -sensitive genotypes derived from crosses between the Cd hyperaccumulator Arabidopsis halleri and Arabidopsis lyrata ssp. petraea. J Exp Bot 57:2967–2983
Craciun AR, Meyer C-L, Chen J et al (2012) Variation in HMA4 gene copy number and expression among Noccaea caerulescens populations presenting different levels of Cd tolerance and accumulation. J Exp Bot 63:4179–4189
Curie C, Cassin G, Couch D et al (2009) Metal movement within the plant: contribution of nicotianamine and Yellow Stripe 1-Like transporters. Ann Bot 103:1–11
De Coninck B, Cammue BPA, Thevissen K (2013) Modes of antifungal action and in planta functions of plant defensins and defensin-like peptides. Fungal Biol Rev 26:109–120
Deinlein U, Weber M, Schmidt H et al (2012) Elevated nicotianamine levels in Arabidopsis halleri roots play a key role in zinc hyperaccumulation. Plant Cell 24:708–723
Delhaize E, Kataoka T, Hebb DM et al (2003) Genes encoding proteins of the cation diffusion facilitator family that confer manganese tolerance. Plant Cell 15:1131–1142
Deng DM, Shu WS, Zhang J et al (2007) Zinc and cadmium accumulation and tolerance in populations of Sedum alfredii. Environ Pollut 147:381–386
Deniau AX, Pieper B, Ten Bookum WM et al (2006) QTL analysis of cadmium and zinc accumulation in the heavy metal hyperaccumulator Thlaspi caerulescens. Theor Appl Genet 113:907–920
Dräger DB, Desbrosses-Fonrouge AG, Krach C et al (2004) Two genes encoding Arabidopsis halleri MTP1 metal transport proteins co-segregate with zinc tolerance and account for high MTP1 transcript levels. Plant J 39:425–439
El Kassis E, Cathala N, Rouached H et al (2007) Characterization of a selenate-resistant Arabidopsis mutant. Root growth as a potential target for selenate toxicity. Plant Physiol 143:1231–1241
Elrashidi MA, Adriano DC, Workman SM, Lindsay WL (1987) Chemical-equilibria of selenium in soils—a theoretical development. Soil Sci 144:141–152
Escarré J, Lefebvre C, Frérot H et al (2013) Metal concentration and metal mass of metallicolous, non metallicolous and serpentine Noccaea caerulescens populations, cultivated in different growth media. Plant Soil 370:197–221
Escarré J, Lefèbvre C, Gruber W et al (2000) Zinc and cadmium hyperaccumulation by Thlaspi caerulescens from metalliferous and nonmetalliferous sites in the Mediterranean area: implications for phytoremediation. New Phytol 145:429–437
Fasani E, DalCorso G, Varotto C et al (2017) The MTP1 promoters from Arabidopsis halleri reveal cis-regulating elements for the evolution of metal tolerance. New Phytol 214:1614–1630
Fernando DR, Bakkaus EJ, Perrier N et al (2006a) Manganese accumulation in the leaf mesophyll of four tree species: a PIXE/EDAX localization study. New Phytol 171:751–757
Fernando DR, Batianoff GN, Baker AJM, Woodrow IE (2006b) In vivo localization of manganese in the hyperaccumulator Gossia bidwillii (Benth.) N. Snow & Guymer (Myrtaceae) by cryo-SEM/EDAX. Plant Cell Env 29:1012–1020
Fernando DR, Marshall A, Baker AJM, Mizuno T (2013) Microbeam methodologies as powerful tools in manganese hyperaccumulation research: present status and future directions. Front Plant Sci 4:9
Fernando DR, Woodrow IE, Baker AJM, Marshall AT (2012) Plant homeostasis of foliar manganese sinks: specific variation in hyperaccumulators. Planta 236:1459–1470
Filatov V, Dowdle J, Smirnoff N et al (2007) A quantitative trait loci analysis of zinc hyperaccumulation in Arabidopsis halleri. New Phytol 174:580–590
Filatov V, Dowdle J, Smirnoff N et al (2006) Comparison of gene expression in segregating families identifies genes and genomic regions involved in a novel adaptation, zinc hyperaccumulation. Mol Ecol 15:3045–3059
Fones H, Davis CAR, Rico A et al (2010) Metal hyperaccumulation armors plants against disease. PLoS Pathog 6:e1001093
Franz KJ (2013) Clawing back: broadening the notion of metal chelators in medicine. Curr Opin Chem Biol 17:143–149
Freeman JL, Tamaoki M, Stushnoff C et al (2010) Molecular mechanisms of selenium tolerance and hyperaccumulation in Stanleya pinnata. Plant Physiol 153:1630–1652
Frérot H, Faucon MP, Willems G et al (2010) Genetic architecture of zinc hyperaccumulation in Arabidopsis halleri: the essential role of QTL x environment interactions. New Phytol 187:355–367
Fukuda N, Kitajima N, Terada Y et al (2020) Visible cellular distribution of cadmium and zinc in the hyperaccumulator Arabidopsis halleri ssp. gemmifera determined by 2-D X-ray fluorescence imaging using high-energy synchrotron radiation. Metallomics 12:193–203
Gao J, Sun L, Yang X, Liu J-X (2013) Transcriptomic analysis of cadmium stress response in the heavy metal hyperaccumulator Sedum alfredii Hance. PLoS ONE 8:e64643
Garcia de la Torre VS, Majorel-Loulergue C, Gonzalez DA et al (2018) Wide cross-species RNA-Seq comparison reveals a highly conserved role for Ferroportins in nickel hyperaccumulation in plants. bioRxiv 420729
Garcia de la Torre VS, Majorel-Loulergue C, Gonzalez DA et al (2020) Wide cross-species RNA-Seq comparison reveals convergent molecular mechanisms involved in nickel hyperaccumulation across dicotyledons. New Phytol https://doi.org/10.1111/nph.16775
Gendre D, Czernic P, Conejero G et al (2007) TcYSL3, a member of the YSL gene family from the hyper-accumulator Thlaspi caerulescens, encodes a nicotianamine-Ni/Fe transporter. Plant J 49:1–15
Ghaderian SM, Ghasemi R, Hajihashemi F (2015) Interaction of nickel and manganese in uptake, translocation and accumulation by the nickel-hyperaccumulator plant, Alyssum bracteatum (Brassicaceae). Aust J Bot 63:47–55
Ghaderian YSM, Lyon AJE, Baker AJM (2000) Seedling mortality of metal hyperaccumulator plants resulting from damping off by Pythium spp. New Phytol 146:219–224
Gonneau C, Genevois N, Frérot H et al (2014) Variation of trace metal accumulation, major nutrient uptake and growth parameters and their correlations in 22 populations of Noccaea caerulescens. Plant Soil 384:271–287
Gustin JL, Loureiro ME, Kim D et al (2009) MTP1-dependent Zn sequestration into shoot vacuole’s suggests dual roles in Zn tolerance and accumulation in Zn hyperaccumulating plants. Plant J 57:1116–1127
Halimaa P, Blande D, Aarts MGM et al (2014a) Comparative transcriptome analysis of the metal hyperaccumulator Noccaea caerulescens. Front Plant Sci 5:213
Halimaa P, Blande D, Baltzi E et al (2019) Transcriptional effects of cadmium on iron homeostasis differ in calamine accessions of Noccaea caerulescens. Plant J 97:306–320
Halimaa P, Lin YF, Ahonen VH et al (2014b) Gene expression differences between Noccaea caerulescens ecotypes help to identify candidate genes for metal phytoremediation. Env Sci Technol 48:3344–3353
Hammond JP, Bowen H, White PJ et al (2006) A comparison of Thlaspi caerulescens and Thlaspi arvense shoot transcriptomes. New Phytol 170:239–260
Han X, Yin H, Song X et al (2016) Integration of small RNAs, degradome and transcriptome sequencing in hyperaccumulator Sedum alfredii uncovers a complex regulatory network and provides insights into cadmium phytoremediation. Plant Biotechnol J 14:1470–1483
Hanikenne M, Baurain D (2014) Origin and evolution of metal p-Type ATPases in Plantae (Archaeplastida). Front Plant Sci 4:544
Hanikenne M, Kroymann J, Trampczynska A et al (2013) Hard selective sweep and ectopic gene conversion in a gene cluster affording environmental adaptation. PLoS Genet 9:e1003707
Hanikenne M, Nouet C (2011) Metal hyperaccumulation and hypertolerance: a model for plant evolutionary genomics. Curr Opin Plant Biol 14:252–259
Hanikenne M, Talke IN, Haydon MJ et al (2008) Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453:391–395
Honjo MN, Kudoh H (2019) Arabidopsis halleri: a perennial model system for studying population differentiation and local adaptation. AoB Plants 11: plz076
Höreth S, Pongrac P, van Elteren JT et al (2020) Arabidopsis halleri shows hyperbioindicator behaviour for Pb and leaf Pb accumulation spatially separated from Zn. New Phytol 226:492–506
Hörger AC, Fones HN, Preston GM (2013) The current status of the elemental defense hypothesis in relation to pathogens. Front Plant Sci 4:395
Hussain D, Haydon MJ, Wang Y et al (2004) P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. Plant Cell 16:1327–1339
Idris R, Kuffner M, Bodrossy L et al (2006) Characterization of Ni-tolerant methylobacteria associated with the hyperaccumulating plant Thlaspi goesingense and description of Methylobacterium goesingense sp. nov. Syst Appl Microbiol 29:634–644
Idris R, Trifonova R, Puschenreiter M et al (2004) Bacterial communities associated with flowering plants of the Ni hyperaccumulator Thlaspi goesingense. Applied Environ Microbiol 70:2667–2677
Ingle RA, Mugford ST, Rees JD et al (2005) Constitutively high expression of the histidine biosynthetic pathway contributes to nickel tolerance in hyperaccumulator plants. Plant Cell 17:2089–2106
Isaure MP, Huguet S, Meyer CL et al (2015) Evidence of various mechanisms of Cd sequestration in the hyperaccumulator Arabidopsis halleri, the non-accumulator Arabidopsis lyrata, and their progenies by combined synchrotron-based techniques. J Exp Bot 66:3201–3214
Kajala K, Walker KL, Mitchell GS et al (2019) Real-time whole-plant dynamics of heavy metal transport in Arabidopsis halleri and Arabidopsis thaliana by gamma-ray imaging. Plant Direct 3:e00131
Karam M-J, Souleman D, Schvartzman MS et al (2019) Genetic architecture of a plant adaptive trait: QTL mapping of intraspecific variation for tolerance to metal pollution in Arabidopsis halleri. Heredity (Edinb) 122:877–892
Kasprzak MM, Erxleben A, Ochocki J (2015) Properties and applications of flavonoid metal complexes. RSC Adv 5:45853–45877
Kerkeb L, Krämer U (2003) The role of free histidine in xylem loading of nickel in Alyssum lesbiacum and Brassica juncea. Plant Physiol 131:716–724
Kim D, Gustin JL, Lahner B et al (2004) The plant CDF family member TgMTP1 from the Ni/Zn hyperaccumulator Thlaspi goesingense acts to enhance efflux of Zn at the plasma membrane when expressed in Saccharomyces cerevisiae. Plant J 39:237–251
Kobayashi T, Nozoye T, Nishizawa NK (2019) Iron transport and its regulation in plants. Free Radic Biol Med 133:11–20
Kopittke PM, Punshon T, Paterson DJ et al (2018) Synchrotron-based X-ray fluorescence microscopy as a technique for imaging of elements in plants. Plant Physiol 178:507–523
Korshunova YO, Eide D, Gregg Clark W et al (1999) The IRT1 protein from Arabidopsis thaliana is a metal transporter with a broad substrate range. Plant Mol Biol 40:37–44
Kozhevnikova AD, Seregin IV, Erlikh NT et al (2014) Histidine-mediated xylem loading of zinc is a species-wide character in Noccaea caerulescens. New Phytol 203:508–519
Krämer U (2010) Metal hyperaccumulation in plants. Annu Rev Plant Biol 61:517–534
Krämer U (2005) MTP1 mops up excess zinc in Arabidopsis cells. Trends Plant Sci 10:313–315
Krämer U, Cotter-Howells JD, Charnock JM et al (1996) Free histidine as a metal chelator in plants that accumulate nickel. Nature 379:635–638
Krämer U, Pickering IJ, Prince RC et al (2000) Subcellular localization and speciation of nickel in hyperaccumulator and non-accumulator Thlaspi species. Plant Physiol 122:1343–1354
Krämer U, Talke IN, Hanikenne M (2007) Transition metal transport. FEBS Lett 581:2263–2272
Krzesłowska M (2011) The cell wall in plant cell response to trace metals: polysaccharide remodeling and its role in defense strategy. Acta Physiol Plant 33:35–51
Küpper H, Lombi E, Zhao FJ et al (2001) Cellular compartmentation of nickel in the hyperaccumulators Alyssum lesbiacum, Alyssum bertolonii and Thlaspi goesingense. J Exp Bot 52:2291–2300
Küpper H, Lombi E, Zhao FJ, McGrath SP (2000) Cellular compartmentation of cadmium and zinc in relation to other elements in the hyperaccumulator Arabidopsis halleri. Planta 212:75–84
Küpper H, Zhao FJ, McGrath SP (1999) Cellular compartmentation of zinc in leaves of the hyperaccumulator Thlaspi caerulescens. Plant Physiol 119:305–311
Lambers H, Hayes PE, Laliberte E et al (2015) Leaf manganese accumulation and phosphorus-acquisition efficiency. Trends Plant Sci 20:83–90
Lasat MM, Pence NS, Garvin DF et al (2000) Molecular physiology of zinc transport in the Zn hyperaccumulator Thlaspi caerulescens. J Exp Bot 51:71–9
Leigh Broadhurst C, Tappero R, Maugel T et al (2009) Interaction of nickel and manganese in accumulation and localization in leaves of the Ni hyperaccumulators Alyssum murale and Alyssum corsicum. Plant Soil 314:35–48
Leitenmaier B, Küpper H (2013) Compartmentation and complexation of metals in hyperaccumulator plants. Front Plant Sci 4:374
Lešková A, Zvarík M, Araya T, Giehl RFH (2019) Nickel toxicity targets cell wall-related processes and PIN2-mediated auxin transport to inhibit root elongation and gravitropic responses in Arabidopsis. Plant Cell Physiol 61:519–535
Li J, Gurajala HK, Wu L et al (2018) Hyperaccumulator plants from China: a synthesis of the current state of knowledge. Environ Sci Technol 52:11980–11994
Li J, Jia Y, Dong R et al (2019) Advances in the mechanisms of plant tolerance to manganese toxicity. Int J Mol Sci 20:5096
Li T, Xu Z, Han X et al (2012) Characterization of dissolved organic matter in the rhizosphere of hyperaccumulator Sedum alfredii and its effect on the mobility of zinc. Chemosphere 88:570–576
Liang J, Shohag MJI, Yang X et al (2014) Role of sulfur assimilation pathway in cadmium hyperaccumulation by Sedum alfredii Hance. Ecotoxicol Environ Saf 100:159–165
Lima LW, Pilon-Smits EAH, Schiavon M (2018) Mechanisms of selenium hyperaccumulation in plants: a survey of molecular, biochemical and ecological cues. Biochim Biophys Acta Gen Subj 1862:2343–2353
Lin YF, Hassan Z, Talukdar S et al (2016) Expression of the ZNT1 zinc transporter from the metal hyperaccumulator Noccaea caerulescens confers enhanced zinc and cadmium tolerance and accumulation to Arabidopsis thaliana. PLoS ONE 11:e0149750
Lin YF, Liang HM, Yang SY et al (2009) Arabidopsis IRT3 is a zinc-regulated and plasma membrane localized zinc/iron transporter. New Phytol 182:392–404
Liu H, Zhao H, Wu L et al (2017) Heavy metal ATPase 3 (HMA3) confers cadmium hypertolerance on the cadmium/zinc hyperaccumulator Sedum plumbizincicola. New Phytol 215:687–698
Lombi E, Zhao F-J, Fuhrmann M et al (2002) Arsenic distribution and speciation in the fronds of the hyperaccumulator Pteris vittata. New Phytol 156:195–203
Losfeld G, L’Huillier L, Fogliani B et al (2015) Leaf age and soil-plant relationships: key factors for reporting trace-elements hyperaccumulation by plants and design applications. Env Sci Pollut Res Int 22:5620–5632
Lu L, Liao X, Labavitch J et al (2014) Speciation and localization of Zn in the hyperaccumulator Sedum alfredii by extended X-ray absorption fine structure and micro-X-ray fluorescence. Plant Physiol Biochem 84:224–232
Lu L, Tian S, Zhang J et al (2013) Efficient xylem transport and phloem remobilization of Zn in the hyperaccumulator plant species Sedum alfredii. New Phytol 198:721–731
Lucisine P, Echevarria G, Sterckeman T et al (2014) Effect of hyperaccumulating plant cover composition and rhizosphere-associated bacteria on the efficiency of nickel extraction from soil. Appl Soil Ecol 81:30–36
Luo S, Chen L, Chen J et al (2011) Analysis and characterization of cultivable heavy metal-resistant bacterial endophytes isolated from Cd-hyperaccumulator Solanum nigrum L. and their potential use for phytoremediation. Chemosphere 85:1130–1138
Ma Y, Prasad MNV, Rajkumar M, Freitas H (2011a) Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnol Adv 29:248–258
Ma Y, Rajkumar M, Luo Y, Freitas H (2011b) Inoculation of endophytic bacteria on host and non-host plants - effects on plant growth and Ni uptake. J Hazard Mater 195:230–237
Mari S, Gendre D, Pianelli K et al (2006) Root-to-shoot long-distance circulation of nicotianamine and nicotianamine-nickel chelates in the metal hyperaccumulator Thlaspi caerulescens. J Exp Bot 57:4111–4122
McNear DH Jr, Chaney RL, Sparks DL (2010) The hyperaccumulator Alyssum murale uses complexation with nitrogen and oxygen donor ligands for Ni transport and storage. Phytochemistry 71:188–200
Meier SK, Adams N, Wolf M et al (2018) Comparative RNA-seq analysis of nickel hyperaccumulating and non-accumulating populations of Senecio coronatus (Asteraceae). Plant J 95:1023–1038
Mengoni A, Pini F, Huang L-N et al (2009a) Plant-by-plant variations of bacterial communities associated with leaves of the nickel hyperaccumulator Alyssum bertolonii Desv. Microb Ecol 58:660–667
Mengoni A, Schat H, Vangronsveld J (2009b) Plants as extreme environments? Ni-resistant bacteria and Ni-hyperaccumulators of serpentine flora. Plant Soil 331:5–16
Menguer PK, Farthing E, Peaston KA et al (2013) Functional analysis of the rice vacuolar zinc transporter OsMTP1. J Exp Bot 64:2871–2883
Merlot S, Hannibal L, Martins S et al (2014) The metal transporter PgIREG1 from the hyperaccumulator Psychotria gabriellae is a candidate gene for nickel tolerance and accumulation. J Exp Bot 65:1551–1564
Meyer C-L, Juraniec M, Huguet S et al (2015) Intraspecific variability of cadmium tolerance and accumulation, and cadmium-induced cell wall modifications in the metal hyperaccumulator Arabidopsis halleri. J Exp Bot 66:3215–3227
Meyer C-L, Kostecka AA, Saumitou-Laprade P et al (2010) Variability of zinc tolerance among and within populations of the pseudometallophyte species Arabidopsis halleri and possible role of directional selection. New Phytol 185:130–142
Meyer C-L, Pauwels M, Briset L et al (2016) Potential preadaptation to anthropogenic pollution: evidence from a common quantitative trait locus for zinc and cadmium tolerance in metallicolous and nonmetallicolous accessions of Arabidopsis halleri. New Phytol 212:934–943
Meyer C-L, Verbruggen N (2012) The use of the model species Arabidopsis halleri towards phytoextraction of cadmium polluted soils. J Biotechnol 30:9–14
Meyer C-L, Vitalis R, Saumitou-Laprade P, Castric V (2009) Genomic pattern of adaptive divergence in Arabidopsis halleri, a model species for tolerance to heavy metal. Mol Ecol 18:2050–2062
Milner MJ, Craft E, Yamaji N et al (2012) Characterization of the high affinity Zn transporter from Noccaea caerulescens, NcZNT1, and dissection of its promoter for its role in Zn uptake and hyperaccumulation. New Phytol 195:113–123
Milner MJ, Kochian LV (2008) Investigating heavy-metal hyperaccumulation using Thlaspi caerulescens as a model system. Ann Bot 102:3–13
Milner MJ, Mitani-Ueno N, Yamaji N et al (2014) Root and shoot transcriptome analysis of two ecotypes of Noccaea caerulescens uncovers the role of NcNramp1 in Cd hyperaccumulation. Plant J 78:398–410
Mirouze M, Sels J, Richard O et al (2006) A putative novel role for plant defensins: a defensin from the zinc hyper-accumulating plant, Arabidopsis halleri, confers zinc tolerance. Plant J 47:329–342
Mizuno T, Usui K, Horie K et al (2005) Cloning of three ZIP/Nramp transporter genes from a Ni hyperaccumulator plant Thlaspi japonicum and their Ni2 + -transport abilities. Plant Physiol Biochem 43:793–801
Mizuno T, Usui K, Nishida S et al (2007) Investigation of the basis for Ni tolerance conferred by the expression of TjZnt1 and TjZnt2 in yeast strains. Plant Physiol Biochem 45:371–378
Molins H, Michelet L, Vi Lanquar et al (2013) Mutants impaired in vacuolar metal mobilization identify chloroplasts as a target for cadmium hypersensitivity in Arabidopsis thaliana. Plant Cell Environ 36:804–817
Molitor M, Dechamps C, Gruber W, Meerts P (2005) Thlaspi caerulescens on nonmetalliferous soil in Luxembourg: ecological niche and genetic variation in mineral element composition. New Phytol 165:503–512
Monsant AC, Kappen P, Wang Y et al (2011) In vivo speciation of zinc in Noccaea caerulescens in response to nitrogen form and zinc exposure. Plant Soil 348:167
Morel M, Crouzet J, Gravot A et al (2009) AtHMA3, a P1B-ATPase allowing Cd/Zn/Co/Pb vacuolar storage in Arabidopsis. Plant Physiol 149:894–904
Morrissey J, Baxter IR, Lee J et al (2009) The ferroportin metal efflux proteins function in iron and cobalt homeostasis in Arabidopsis. Plant Cell 21:3326–3338
Muehe EM, Weigold P, Adaktylou IJ et al (2015) Rhizosphere microbial community composition affects cadmium and zinc uptake by the metal-hyperaccumulating plant Arabidopsis halleri. Appl Environ Microbiol 81:2173–2181
Nguyen NNT, Ranwez V, Vile D et al (2014) Evolutionary tinkering of the expression of PDF1s suggests their joint effect on zinc tolerance and the response to pathogen attack. Front Plant Sci 5:70
Nishida S, Aisu A, Mizuno T (2012) Induction of IRT1 by the nickel-induced iron-deficient response in Arabidopsis. Plant Signal Behav 7:329–331
Nishida S, Tsuzuki C, Kato A et al (2011) AtIRT1, the primary iron uptake transporter in the root, mediates excess nickel accumulation in Arabidopsis thaliana. Plant Cell Physiol 52:1433–1442
Nouet C, Charlier JB, Carnol M et al (2015) Functional analysis of the three HMA4 copies of the metal hyperaccumulator Arabidopsis halleri. J Exp Bot 66:5783–5795
Nowak J, Frérot H, Faure N et al (2018) Can zinc pollution promote adaptive evolution in plants? Insights from a one-generation selection experiment. J Exp Bot 69:5561–5572
O’ Lochlainn S, Bowen HC, Fray RG, et al (2011) Tandem quadruplication of HMA4 in the zinc (Zn) and cadmium (Cd) hyperaccumulator Noccaea caerulescens. PLoS One 6:e17814
Oomen RJ, Seveno-Carpentier E, Ricodeau N et al (2011) Plant defensin AhPDF1.1 is not secreted in leaves but it accumulates in intracellular compartments. New Phytol 192:140–150
Oomen RJFJ, Wu J, Lelièvre F et al (2009) Functional characterization of NRAMP3 and NRAMP4 from the metal hyperaccumulator Thlaspi caerulescens. New Phytol 181:637–65
Paape T, Briskine RV, Halstead-Nussloch G et al (2018) Patterns of polymorphism and selection in the subgenomes of the allopolyploid Arabidopsis kamchatica. Nat Commun 9:3909
Pankievicz VC, Camilios-Neto D, Bonato P et al (2016) RNA-seq transcriptional profiling of Herbaspirillum seropedicae colonizing wheat (Triticum aestivum) roots. Plant Mol Biol 90:589–603
Papoyan A, Kochian LV (2004) Identification of Thlaspi caerulescens genes that may be involved in heavy metal hyperaccumulation and tolerance. Characterization of a novel heavy metal transporting ATPase. Plant Physiol 136:3814–3823
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 (Brassicaceae). J Evol Biol 19:1838–1850
Pauwels M, Roosens N, Frérot H, Saumitou-Laprade P (2008) When population genetics serves genomics: putting adaptation back in a spatial and historical context. Curr Opin Plant Biol 11:129–134
Pauwels M, Vekemans X, Godé C et al (2012) Nuclear and chloroplast DNA phylogeography reveals vicariance among European populations of the model species for the study of metal tolerance, Arabidopsis halleri (Brassicaceae). New Phytol 193:916–928
Pedersen CNS, Axelsen KB, Harper JF, Palmgren MG (2012) Evolution of plant P-type ATPases. Front Plant Sci 3:31
Peer WA, Mamoudian M, Lahner B et al (2003) Identifying model metal hyperaccumulating plants: germplasm analysis of 20 Brassicaceae accessions from a wide geographical area. New Phytol 159:421–430
Pence NS, Larsen PB, Ebbs SD et al (2000) The molecular physiology of heavy metal transport in the Zn/Cd hyperaccumulator Thlaspi caerulescens. Proc Natl Acad Sci USA 97:4956–60
Peng JS, Wang YJ, Ding G et al (2017) A pivotal role of cell wall in cadmium accumulation in the Crassulaceae hyperaccumulator Sedum plumbizincicola. Mol Plant 10:771–774
Persans MW, Nieman K, Salt DE (2001) Functional activity and role of cation-efflux family members in Ni hyperaccumulation in Thlaspi goesingense. Proc Natl Acad Sci USA 98:9995–10000
Persans MW, Yan X, Patnoe JM et al (1999) Molecular dissection of the role of histidine in nickel hyperaccumulation in Thlaspi goesingense (Halácsy). Plant Physiol 121:1117–1126
Pianelli K, Mari S, Marques L et al (2005) Nicotianamine over-accumulation confers resistance to nickel in Arabidopsis thaliana. Transgenic Res 14:739–748
Pickering IJ, Wright C, Bubner B et al (2003) Chemical form and distribution of selenium and sulfur in the selenium hyperaccumulator Astragalus bisulcatus. Plant Physiol 131:1460–1467
Pittman JK (2005) Managing the manganese: molecular mechanisms of manganese transport and homeostasis. New Phytol 167:733–742
Polacco JC, Mazzafera P, Tezotto T (2013) Opinion- Nickel and urease in plants: still many knowledge gaps. Plant Sci 199–200:79–90
Pongrac P, Serra TS, Castillo-Michel H et al (2018) Cadmium associates with oxalate in calcium oxalate crystals and competes with calcium for translocation to stems in the cadmium bioindicator Gomphrena claussenii. Metallomics 10:1576–1584
Pottier M, Oomen R, Picco C et al (2015) Identification of mutations allowing Natural Resistance Associated Macrophage Proteins (NRAMP) to discriminate against cadmium. Plant J 83:625–637
Preite V, Sailer C, Syllwasschy L et al (2019) Convergent evolution in Arabidopsis halleri and Arabidopsis arenosa on calamine metalliferous soils. Philos Trans R Soc B Biol Sci 374:20180243
Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci 180:169–181
Reeves RD, Baker AJM, Jaffré T et al (2018) A global database for plants that hyperaccumulate metal and metalloid trace elements. New Phytol 218:407–411
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 3:145–172
Reinhold-Hurek B, Hurek T (2011) Living inside plants: bacterial endophytes. Curr Opin Plant Biol 14:435–443
Rellan-Alvarez R, Abadia J, Alvarez-Fernandez A (2008) Formation of metal-nicotianamine complexes as affected by pH, ligand exchange with citrate and metal exchange. A study by electrospray ionization time-of-flight mass spectrometry. Rapid Commun Mass Spectrom 22:1553–1562
Reynolds RJB, Pilon-Smits EAH (2018) Plant selenium hyperaccumulation—ecological effects and potential implications for selenium cycling and community structure. Biochim Biophys Acta Gen Subj 1862:2372–2382
Ricachenevsky FK, Menguer PK, Sperotto RA, Fett JP (2015) Got to hide your Zn away: molecular control of Zn accumulation and biotechnological applications. Plant Sci 236:1–17
Richau KH, Kozhevnikova AD, Seregin IV et al (2009) Chelation by histidine inhibits the vacuolar sequestration of nickel in roots of the hyperaccumulator Thlaspi caerulescens. New Phytol 183:106–116
Rogers EE, Eide DJ, Guerinot ML (2000) Altered selectivity in an Arabidopsis metal transporter. Proc Natl Acad Sci USA 97:12356–12360
Rogers EE, Guerinot ML (2002) FRD3, a member of the multidrug and toxin efflux family, controls iron deficiency responses in Arabidopsis. Plant Cell 14:1787–1799
Roosens N, Verbruggen N, Meerts P et al (2003) Natural variation in cadmium hyperaccumulation and its relationship to metal hyperaccumulation for seven populations of Thlaspi caerulescens from western Europe. Plant Cell Env 26:1657–1672
Roosens NH, Willems G, Saumitou-Laprade P (2008) Using Arabidopsis to explore zinc tolerance and hyperaccumulation. Trends Plant Sci 13:208–215
Roux C, Castric V, Pauwels M et al (2011) Does speciation between Arabidopsis halleri and Arabidopsis lyrata coincide with major changes in a molecular target of adaptation? PLoS ONE 6:e26872
Sailer C, Babst-Kostecka A, Fischer MC et al (2018) Transmembrane transport and stress response genes play an important role in adaptation of Arabidopsis halleri to metalliferous soils. Sci Rep 8:16085
Sarret G, Saumitou-Laprade P, Bert V et al (2002) Forms of zinc accumulated in the hyperaccumulator Arabidopsis halleri. Plant Physiol 130:1815–1826
Sarret G, Smits E, Michel HC et al (2013) Use of synchrotron-based techniques to elucidate metal uptake and metabolism in plants. In: Sparks DL (ed) Advances in Agronomy, vol 119. Elsevier Academic Press Inc, San Diego, pp 1–82
Sarret G, Willems G, Isaure MP et al (2009) Zinc distribution and speciation in Arabidopsis halleri x Arabidopsis lyrata progenies presenting various zinc accumulation capacities. New Phytol 184:581–595
Schaaf G, Honsbein A, Meda AR et al (2006) AtIREG2 encodes a tonoplast transport protein involved in iron-dependent nickel detoxification in Arabidopsis thaliana roots. J Biol Chem 281:25532–25540
Schaumlöffel D, Ouerdane L, Bouyssiere B, Lobinski R (2003) Speciation analysis of nickel in the latex of a hyperaccumulating tree Sebertia acuminata by HPLC and CZE with ICP MS and electrospray MS-MS detection. J Anal At Spectrom 18:120–127
Schiavon M, Pilon-Smits EAH (2017) The fascinating facets of plant selenium accumulation—biochemistry, physiology, evolution and ecology. New Phytol 213:1582–1596
Schiavon M, Pilon M, Malagoli M, Pilon-Smits EAH (2015) Exploring the importance of sulfate transporters and ATP sulphurylases for selenium hyperaccumulation—a comparison of Stanleya pinnata and Brassica juncea (Brassicaceae). Front Plant Sci 6:1–13
Schvartzman MS, Corso M, Fataftah N et al (2018) Adaptation to high zinc depends on distinct mechanisms in metallicolous populations of Arabidopsis halleri. New Phytol 218:269–282
Sessitsch A, Hardoim P, Döring J et al (2012) Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. Mol Plant Microbe Interact 25:28–36
Shahzad Z, Gosti F, Frérot H et al (2010) The five AhMTP1 zinc transporters undergo different evolutionary fates towards adaptive evolution to zinc tolerance in Arabidopsis halleri. PLoS Genet 6:e1000911
Shahzad Z, Ranwez V, Fizames C et al (2013) Plant Defensin type 1 (PDF1): protein promiscuity and expression variation within the Arabidopsis genus shed light on zinc tolerance acquisition in Arabidopsis halleri. New Phytol 200:820–833
Shao JF, Yamaji N, Shen RF, Ma JF (2017) The key to Mn homeostasis in plants: regulation of Mn transporters. Trends Plant Sci 22:215–224
Shibagaki N, Rose A, McDermott JP et al (2002) Selenate-resistant mutants of Arabidopsis thaliana identify Sultr1;2, a sulfate transporter required for efficient transport of sulfate into roots. Plant J 29:475–486
Socha AL, Guerinot ML (2014) Mn-euvering manganese: the role of transporter gene family members in manganese uptake and mobilization in plants. Front Plant Sci 5:106
Spielmann J, Ahmadi H, Scheepers M et al (2020) The two copies of the zinc and cadmium ZIP6 transporter of Arabidopsis halleri have distinct effects on cadmium tolerance. Plant Cell Environ 43:2143–2157
Stein RJ, Höreth S, de Melo JRF et al (2017) Relationships between soil and leaf mineral composition are element-specific, environment-dependent and geographically structured in the emerging model Arabidopsis halleri. New Phytol 213:1274–1286
Sterckeman T, Cazes Y, Sirguey C (2019) Breeding the hyperaccumulator Noccaea caerulescens for trace metal phytoextraction: first results of a pure-line selection. Int J Phytoremediation 21:448–455
Suryawanshi V, Talke IN, Weber M et al (2016) Between-species differences in gene copy number are enriched among functions critical for adaptive evolution in Arabidopsis halleri. BMC Genom 17:1034
Szopiński M, Sitko K, Gieroń Ż et al (2019) Toxic effects of Cd and Zn on the photosynthetic apparatus of the Arabidopsis halleri and Arabidopsis arenosa pseudo-metallophytes. Front Plant Sci 10:748
Takahashi H, Watanabe-Takahashi A, Smith FW et al (2000) The roles of three functional sulphate transporters involved in uptake and translocation of sulphate in Arabidopsis thaliana. Plant J 23:171–182
Talke IN, Hanikenne M, Krämer U (2006) Zinc-dependent global transcriptional control, transcriptional deregulation, and higher gene copy number for genes in metal homeostasis of the hyperaccumulator Arabidopsis halleri. Plant Physiol 142:148–167
Thomine S, Vert G (2013) Iron transport in plants: better be safe than sorry. Curr Opin Plant Biol 16:322–327
Tian S, Lu L, Labavitch J et al (2011) Cellular sequestration of cadmium in the hyperaccumulator plant species Sedum alfredii. Plant Physiol 157:1914–1925
Tsednee M, Yang S-C, Lee D-C, Yeh K-C (2014) Root-secreted nicotianamine from Arabidopsis halleri facilitates zinc hypertolerance by regulating zinc bioavailability. Plant Physiol 166:839–852
Turner TL, Bourne EC, Von Wettberg EJ et al (2010) Population resequencing reveals local adaptation of Arabidopsis lyrata to serpentine soils. Nat Genet 42:260–263
Ueno D, Milner MJ, Yamaji N et al (2011) Elevated expression of TcHMA3 plays a key role in the extreme Cd tolerance in a Cd-hyperaccumulating ecotype of Thlaspi caerulescens. Plant J 66:852–862
Uraguchi S, Weber M, Clemens S (2019) Elevated root nicotianamine concentrations are critical for Zn hyperaccumulation across diverse edaphic environments. Plant, Cell Environ 42:2003–2014
van de Mortel JE, Almar Villanueva L, Schat H et al (2006) Large expression differences in genes for iron and zinc homeostasis, stress response, and lignin biosynthesis distinguish roots of Arabidopsis thaliana and the related metal hyperaccumulator Thlaspi caerulescens. Plant Physiol 142:1127–1147
van de Mortel JE, Schat H, Moerland PD et al (2008) Expression differences for genes involved in lignin, glutathione and sulphate metabolism in response to cadmium in Arabidopsis thaliana and the related Zn/Cd-hyperaccumulator Thlaspi caerulescens. Plant Cell Env 31:301–324
van der Ent A, Baker AJM, Reeves RD et al (2013) Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant Soil 362:319–334
van der Ent A, Przybyłowicz WJ, de Jonge MD et al (2018) X-ray elemental mapping techniques for elucidating the ecophysiology of hyperaccumulator plants. New Phytol 218:432–452
van der Ent A, Spiers KM, Brueckner D et al (2019) Spatially-resolved localization and chemical speciation of nickel and zinc in Noccaea tymphaea and Bornmuellera emarginata. Metallomics 11:2052–2065
van der Pas L, Ingle AR (2019) Towards an understanding of the molecular basis of nickel hyperaccumulation in plants. Plants 8:11
van der Weerden NL, Anderson MA (2013) Plant defensins: Common fold, multiple functions. Fungal Biol Rev 26:121–131
Verbruggen N, Hanikenne M, Clemens S (2013a) A more complete picture of metal hyperaccumulation through next-generation sequencing technologies. Front Plant Sci 4:388
Verbruggen N, Hermans C, Schat H (2009) Molecular mechanisms of metal hyperaccumulation in plants. New Phytol 181:759–776
Verbruggen N, Juraniec M, Baliardini C, Meyer C-L (2013b) Tolerance to cadmium in plants: the special case of hyperaccumulators. Biometals 26:633–638
Vert G, Grotz N, Dedaldechamp F et al (2002) IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14:1223–1233
Villafort Carvalho MT, Amaral DC, Guilherme LR, Aarts MGM (2013) Gomphrena claussenii, the first South-American metallophyte species with indicator-like Zn and Cd accumulation and extreme metal tolerance. Front Plant Sci 4:180
Villafort Carvalho MT, Pongrac P, Mumm R et al (2015) Gomphrena claussenii, a novel metal-hypertolerant bioindicator species, sequesters cadmium, but not zinc, in vacuolar oxalate crystals. New Phytol 208:763–775
Visioli G, D’Egidio S, Vamerali T et al (2014) Culturable endophytic bacteria enhance Ni translocation in the hyperaccumulator Noccaea caerulescens. Chemosphere 117:538–544
Visioli G, Vamerali T, Mattarozzi M et al (2015) Combined endophytic inoculants enhance nickel phytoextraction from serpentine soil in the hyperaccumulator Noccaea caerulescens. Front Plant Sci 6:1–12
Wang J, Cappa JJ, Harris JP et al (2018) Transcriptome-wide comparison of selenium hyperaccumulator and nonaccumulator Stanleya species provides new insight into key processes mediating the hyperaccumulation syndrome. Plant Biotechnol J 16:1582–1594
Wang J, Xiong Y, Zhang J et al (2020) Naturally selected dominant weeds as heavy metal accumulators and excluders assisted by rhizosphere bacteria in a mining area. Chemosphere 243:125365
Weber M, Harada E, Vess C et al (2004) Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors. Plant J 37:269–281
Weber M, Trampczynska A, Clemens S (2006) Comparative transcriptome analysis of toxic metal responses in Arabidopsis thaliana and the Cd2 + -hypertolerant facultative metallophyte Arabidopsis halleri. Plant Cell Env 29:950–963
Wei W, Chai T, Zhang Y et al (2009) The Thlaspi caerulescens NRAMP homologue TcNRAMP3 is capable of divalent cation transport. Mol Biotechnol 41:15–21
White PJ (2016) Selenium accumulation by plants. Ann Bot 117:217–235
Willems G, Dräger DB, Courbot M et al (2007) The genetic basis of zinc tolerance in the metallophyte Arabidopsis halleri ssp. halleri (Brassicaceae): an analysis of quantitative trait loci. Genetics 176:659–674
Willems G, Frérot H, Gennen J et al (2010) Quantitative trait loci analysis of mineral element concentrations in an Arabidopsis halleri x Arabidopsis lyrata petraea F2 progeny grown on cadmium-contaminated soil. New Phytol 187:368–379
Wong CKE, Cobbett CS (2009) HMA P-type ATPases are the major mechanism for root-to-shoot Cd translocation in Arabidopsis thaliana. New Phytol 181:71–78
Wu J, Zhao F-J, Ghandilyan A et al (2009) Identification and functional analysis of two ZIP metal transporters of the hyperaccumulator Thlaspi caerulescens. Plant Soil 325:79
Wu LH, Liu YJ, Zhou SB et al (2013) Sedum plumbizincicola X.H. Guo et S.B. Zhou ex L.H. Wu (Crassulaceae): A new species from Zhejiang Province, China. Plant Syst Evol 299:487–498
Wu Y, Ma L, Liu Q et al (2020a) The plant-growth promoting bacteria promote cadmium uptake by inducing a hormonal crosstalk and lateral root formation in a hyperaccumulator plant Sedum alfredii. J Hazard Mater 395:122661
Wu Y, Ma L, Liu Q et al (2020b) Pseudomonas fluorescens promote photosynthesis, carbon fixation and cadmium phytoremediation of hyperaccumulator Sedum alfredii. Sci Total Environ 726:138554
Wycisk K, Kim EJ, Schroeder JI, Krämer U (2004) Enhancing the first enzymatic step in the histidine biosynthesis pathway increases the free histidine pool and nickel tolerance in Arabidopsis thaliana. FEBS Lett 578:128–134
Yang X, Li T, Yang J et al (2006) Zinc compartmentation in root, transport into xylem, and absorption into leaf cells in the hyperaccumulating species of Sedum alfredii Hance. Planta 224:185–195
Yang XE, Long XX, Ye HB et al (2004) Cadmium tolerance and hyperaccumulation in a new Zn-hyperaccumulating plant species (Sedum alfredii Hance). Plant Soil 259:181–189
Yang Q, Ma X, Luo S et al (2018) SaZIP4, an uptake transporter of Zn/Cd hyperaccumulator Sedum alfredii Hance. Environ Exp Bot 155:107–117
Yang Q, Shohag MJI, Feng Y et al (2017) Transcriptome comparison reveals the adaptive evolution of two contrasting ecotypes of Zn/Cd hyperaccumulator Sedum alfredii Hance . Front Plant Sci 8:425
Yogeeswaran K, Frary A, York TL et al (2005) Comparative genome analyses of Arabidopsis spp.: Inferring chromosomal rearrangement events in the evolutionary history of A. thaliana. Genome Res 15:505–515
Yokosho K, Yamaji N, Ueno D et al (2009) OsFRDL1 is a citrate transporter required for efficient translocation of iron in rice. Plant Physiol 149:297–305
Zhang L, Hu B, Li W et al (2014) OsPT2, a phosphate transporter, is involved in the active uptake of selenite in rice. New Phytol 201:1183–91
Zhang M, Senoura T, Yang X, Nishizawa NK (2011) Functional analysis of metal tolerance proteins isolated from Zn/Cd hyperaccumulating ecotype and non-hyperaccumulating ecotype of Sedum alfredii Hance. FEBS Lett 585:2604–2609
Zhang Z, Yu Q, Du H et al (2016) Enhanced cadmium efflux and root-to-shoot translocation are conserved in the hyperaccumulator Sedum alfredii (Crassulaceae family). FEBS Lett 590:1757–1764
Zhao XQ, Mitani N, Yamaji N et al (2010) Involvement of silicon influx transporter OsNIP2;1 in selenite uptake in rice. Plant Physiol 153:1871–1877
Zhao H, Wang L, Zhao F-J et al (2019) SpHMA1 is a chloroplast cadmium exporter protecting photochemical reactions in the Cd hyperaccumulator Sedum plumbizincicola. Plant Cell Environ 42:1112–1124
Zhu YG, Pilon-Smits EA, Zhao FJ et al (2009) Selenium in higher plants: understanding mechanisms for biofortification and phytoremediation. Trends Plant Sci 14:436–442
Acknowledgements
We thank colleagues in our laboratories for critical reading of the manuscript. The research of SM and VSGT was supported by the French National Research Agency (ANR-13-ADAP-0004) and by CNRS (Defi Enviromics and Defi X-Life). Funding to MH is from the ‘Fonds de la Recherche Scientifique–FNRS’ (PDR-T.0206.13, MIS-F.4511.16, CDR J.0009.17, PDR-T0120.18) and the University of Liège (SFRD-12/03, ARC GreenMagic). MH is a Senior Research Associate of the FNRS.
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Merlot, S., Garcia de la Torre, V.S., Hanikenne, M. (2021). Physiology and Molecular Biology of Trace Element Hyperaccumulation. In: van der Ent, A., Baker, A.J., Echevarria, G., Simonnot, MO., Morel, J.L. (eds) Agromining: Farming for Metals. Mineral Resource Reviews. Springer, Cham. https://doi.org/10.1007/978-3-030-58904-2_8
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