Abstract
Research reported by Liu et al. in this issue shows that hyperaccumulation of rare earth elements (REEs) in Phytolacca americana occurs because its roots release carboxylates and lower the pH of the rhizosphere. The main function of carboxylate release in this species appears to be enhanced uptake of phosphorus (P). The idea that REE hyperaccumulation may have arisen as a side-effect of P acquisition is an example of the “inadvertent uptake” hypothesis for hyperaccumulation. In this Commentary, I consider the extent to which similar processes may be widely important among all hyperaccumulators. There are some relatively unspecialized hyperaccumulator species, like P. americana, which accumulate multiple elements and grow on a wide range of soils, most of which are not unusually enriched in any elements. It may be that carboxylate release explains the physiological functioning of these plants, at least in part. However, most hyperaccumulators are more specialized, accumulating specific elements and occurring exclusively on metalliferous soils. In such species, current evidence suggests that hyperaccumulation is more dependent on the plants’ internal mechanisms of elemental transport, sequestration, and detoxification than on rhizosphere processes. Nonetheless, inadvertent uptake as a consequence of P- acquisition mechanisms may have been an important starting point in the evolution of such lineages.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
No original data are reported in this article.
References
Alford ÉR, Pilon-Smits EAH, Paschke MW (2010) Metallophytes – a view from the rhizosphere. Plant Soil 337:33–50. https://doi.org/10.1007/s11104-010-0482-3
Álvarez-Fernández A, Díaz-Benito P, Abadía A, López-Millán AF, Abadía J (2014) Metal species involved in long distance metal transport in plants. Front Plant Sci 5:105. https://doi.org/10.3389/fpls.2014.00105
Assunção AGL, Schat H, Aarts MGM (2003) Thlaspi caerulescens, an attractive model species to study heavy metal hyperaccumulation in plants. New Phytol 159(2):351–360. https://doi.org/10.1046/j.1469-8137.2003.00820.x
Bernal MP, McGrath SP (1994) Effects of pH and heavy-metal concentrations in solution culture on the proton release, growth and elemental composition of Alyssum murale and Raphanus sativus L. Plant Soil 166:83–92. https://doi.org/10.1007/BF02185484
Bettarini I, Gonnelli C, Selvi F, Coppi A, Pazzagli L, Colzi I (2021) Diversity of Ni growth response and accumulation in Central-Eastern Mediterranean Odontarrhena (Brassicaceae) populations on and off serpentine sites. Environ Exp Bot 186:104455. https://doi.org/10.1016/j.envexpbot.2021.104455
Boyd RS, Martens SN (1992) The raison d’être for metal hyperaccumulation by plants. In: Baker AJM, Proctor J, Reeves RD (eds) The vegetation of ultramafic (serpentine) soils. Intercept, Andover, pp 279–289
Chaney RL, Baker AJM, Morel JL (2021) The long road to developing agromining/phytomining. In: van der Ent A, Baker AJM, Echevarria G, Simonnot M-O, Morel JL (eds) Agromining: Farming for Metals, 2nd edn. Mineral Resource Reviews, Springer International Publishing, Cham, pp 1–22
Chen C, Zhang HX, Wang AG, Lu M, Shen ZG, Lian CL (2015) Phenotypic plasticity accounts for most of the variation in leaf manganese concentrations in Phytolacca americana growing in manganese-contaminated environments. Plant Soil 396:215–227. https://doi.org/10.1007/s11104-015-2581-7
Chen ZQ, Chen ZB, Yan XY, Bai LY (2016) Stoichiometric mechanisms of Dicranopteris dichotoma, growth and resistance to nutrient limitation in the Zhuxi watershed in the red soil hilly region of China. Plant Soil 398:367–379. https://doi.org/10.1007/s11104-015-2670-7
Chen YT, Wang Y, Yeh KC (2017) Role of root exudates in metal acquisition and tolerance. Curr Opin Plant Biol 39:66–72. https://doi.org/10.1016/j.pbi.2017.06.004
Chen HB, Chen HM, Chen ZB (2022) A review of in situ phytoextraction of rare earth elements from contaminated soils. Int J Phytorem 24:557–566. https://doi.org/10.1080/15226514.2021.1957770
DeGroote KV, McCartha GL, Pollard AJ (2018) Interactions of the manganese hyperaccumulator Phytolacca americana L. with soil pH and phosphate. Ecol Res 33:749–755. https://doi.org/10.1007/s11284-017-1547-z
Delgado M, Valle S, Barra PJ, Reyes-Diáz M, Zúñiga-Feest A (2019) New aluminum hyperaccumulator species of the Proteaceae family from southern South America. Plant Soil 444:475–487. https://doi.org/10.1007/s11104-019-04289-2
Deng THB, van der Ent A, Tan YT, Sterckeman T, Echevarria G, Morel JL, Qiu RL (2018) Nickel hyperaccumulation mechanisms: a review on the current state of knowledge. Plant Soil 423:1–11. https://doi.org/10.1007/s11104-017-3539-8
Denton MD, Veneklaas EJ, Lambers H (2007) Does phenotypic plasticity in carboxylate exudation differ among rare and widespread Banksia species (Proteaceae)? New Phytol 173:592–599. https://doi.org/10.1111/j.1469-8137.2006.01956.x
Do C, Abubakari F, Remigio AC, Brown GK, Casey LW, Sarramegna VB, Gei V, Erskine PD, van der Ent A (2020) A preliminary survey of nickel, manganese and zinc (hyper)accumulation in the flora of Papua New Guinea from herbarium X-ray fluorescence scanning. Chemoecology 30:1–13. https://doi.org/10.1007/s00049-019-00293-1
Fernando DR, Guymer G, Reeves RD, Woodrow IE, Baker AJ, Batianoff GN (2009) Foliar Mn accumulation in eastern Australian herbarium specimens: Prospecting for ‘new’ Mn hyperaccumulators and its potential application in taxonomy. Ann Bot 103:931–939. https://doi.org/10.1016/j.envexpbot.2021.104668
Gao L, Peng K, Xia Y, Wang G, Niu L, Lian C, Shen Z (2013) Cadmium and manganese accumulation in Phytolacca americana L. and the roles of non-protein thiols and organic acids. Int J Phytorem 15:307–319. https://doi.org/10.1080/15226514.2012.702800
García de la Torre V, Majorel-Loulergue C, Rigaill GJ et al (2021) Wide cross-species RNA-Seq comparison reveals convergent molecular mechanisms involved in nickel hyperaccumulation across dicotyledons. New Phytol 229:994–1006. https://doi.org/10.1111/nph.16775
Gardner WK, Parbery DG, Barber DA (1981) Proteoid root morphology and function in Lupinus albus. Plant Soil 60:143–147. https://doi.org/10.1007/BF02377120
Gardner WK, Parbery DG, Barber DA (1982) The acquisition of phosphorus by Lupinus albus L. II. The effect of varying phosphorus supply and soil type on some characteristics of the soil/root interface. Plant Soil 68:33–41. https://doi.org/10.1007/BF02374754
Gei V, Isnard S, Erskine PD, Echevarria G, Fogliani B, Jaffré T, van der Ent A (2020) A systematic assessment of the occurrence of trace element hyperaccumulation in the flora of New Caledonia. Bot J Linn Soc 194:1–22. https://doi.org/10.1093/botlinnean/boaa029
Grosjean N, Le Jean M, Berthelot C, Chalot M, Gross EM, Blaudez D (2019) Accumulation and fractionation of rare earth elements are conserved traits in the Phytolacca genus. Sci Rep 9:18458. https://doi.org/10.1038/s41598-019-54238-3
Haydon MJ, Cobbett CS (2007) Transporters of ligands for essential metal ions in plants. New Phytol 174:499–506. https://doi.org/10.1111/j.1469-8137.2007.02051.x
Hörger AC, Fones HN, Preston GM (2013) The current status of the elemental defense hypothesis in relation to pathogens. Front Plant Sci 4:395. https://doi.org/10.3389/fpls.2013.00395
Hutchinson JJ, Young SD, McGrath SP, West HM, Black CR, Baker AJM (2000) Determining uptake of ‘non-labile’ soil cadmium by Thlaspi caerulescens using isotopic dilution techniques. New Phytol 146:453–460. https://doi.org/10.1046/j.1469-8137.2000.00657.x
Ichihashi H, Morita H, Tatsukawa R (1992) Rare earth elements (REEs) in naturally grown plants in relation to their variation in soils. Environ Pollut 76:157–162. https://doi.org/10.1016/0269-7491(92)90103-H
Invernón VR, Tisserand R, Jouannais P, Navarrete Gutiérrez DM, Muller S, Pillon Y, Echevarria G, Merlot S (2021) The discovery of new metal-hyperaccumulating plant species in herbaria. In: Pellens R (ed) Natural History Collections in the Science of the 21st Century: A Sustainable Resource for Open Science. John Wiley & Sons, pp 79–94
Jansen S, Broadley MR, Robbrecht E, Smets E (2002) Aluminum hyperaccumulation in angiosperms: a review of its phylogenetic significance. Bot Rev 68:235–269. https://doi.org/10.1663/0006-8101(2002)068[0235:AHIAAR]2.0.CO;2
Jansen S, Watanabe T, Dessein S, Smets E, Robbrecht E (2003) A comparative study of metal levels in leaves of some Al-accumulating Rubicaceae. Ann Bot 91:657–663. https://doi.org/10.1093/aob/mcg071
Kidd PS, Becerra-Castro C, García-Lestón M, Monterroso C (2007) Aplicación de plantas hiperacumuladoras de níquel en la fitoextracción natural: el género Alyssum L. Ecosistemas 16:26–43. https://www.revistaecosistemas.net/index.php/ecosistemas/article/view/126. Accessed 26 Dec 2022
Lai Y, Wang Q, Yang L, Huang B (2006) Subcellular distribution of rare earth elements and characterization of their binding species in a newly discovered hyperaccumulator Pronephrium simplex. Talanta 70:26–31. https://doi.org/10.1016/j.talanta.2005.12.062
Lambers H (2022) Phosphorus acquisition and utilization in plants. Annu Rev Plant Biol 73:17–42. https://doi.org/10.1146/annurev-arplant-102720-125738
Lambers H, Clements JC, Nelson MN (2013) How a phosphorus-acquisition strategy based on carboxylate exudation powers the success and agronomic potential of lupines (Lupinus, Fabaceae). Am J Bot 100(2):263–288. https://doi.org/10.3732/ajb.1200474
Lambers H, Hayes PE, Laliberte E, Oliveira RS, Turner BL (2015) Leaf manganese accumulation and phosphorus-acquisition efficiency. Trends Plant Sci 20:83–90. https://doi.org/10.1016/j.tplants.2014.10.007
Lambers H, Wright IJ, Pereira CG et al (2021) Leaf manganese concentrations as a tool to assess belowground plant functioning in phosphorus-impoverished environments. Plant Soil 461:43–61. https://doi.org/10.1007/s11104-020-04690-2
Lambers H, de Britto CP, Cawthray GR et al (2022) Strategies to acquire and use phosphorus in phosphorus-impoverished and fire-prone environments. Plant Soil 476:133–160. https://doi.org/10.1007/s11104-022-05464-8
Liu P, Tang X, Gong C, Xu G (2010) Manganese tolerance and accumulation in six Mn hyperaccumulators or accumulators. Plant Soil 335:385–395. https://doi.org/10.1007/s11104-010-0427-x
Liu C, Liu WS, van der Ent A, Morel JL, Zheng HX, Wang GB, Tang YT, Qiu RL (2021a) Simultaneous hyperaccumulation of rare earth elements, manganese and aluminum in Phytolacca americana in response to soil properties. Chemosphere 282:131096. https://doi.org/10.1016/j.chemosphere.2021.131096
Liu WS, Zheng HX, Liu C, Guo MN, Zhu SC, Cao Y, Qiu RL, Morel JL, van der Ent A, Tang YT (2021b) Variation in rare earth elements (REE), aluminium (Al) and silicon (Si) accumulation among populations of the hyperaccumulator Dicranopteris linearis in southern China. Plant Soil 461:565–578. https://doi.org/10.1007/s11104-021-04835-x
Liu C, Ding TX, Liu WS, Tang YT, Qiu RL (2023) Phosphorus mediated rhizosphere mobilization and apoplast precipitation regulate rare earth element accumulation in Phytolacca americana. Plant Soil. https://doi.org/10.1007/s11104-022-05743-4
Luo YM, Christie P, Baker AJM (2000) Soil solution Zn and pH dynamics in non-rhizosphere soil and in the rhizosphere of Thlaspi caerulescens grown in a Zn/Cd contaminated soil. Chemosphere 41:161–164. https://doi.org/10.1016/S0045-6535(99)00405-1
Luo Q, Wang S, Sun LN, Wang H (2017) Metabolic profiling of root exudates from two ecotypes of Sedum alfredii treated with Pb based on GC-MS. Sci Rep 7:39878. https://doi.org/10.1038/srep39878
Ma X, Mason-Jones K, Liu Y, Blagodatskaya E, Kuzyakov Y, Guber A, Dippold M, Razavi B (2019) Coupling zymography with pH mapping reveals a shift in lupine phosphorus acquisition strategy driven by cluster roots. Soil Biol Biochem 135:420–428. https://doi.org/10.1016/j.soilbio.2019.06.001
Magalhaes JV, Piñeros MA, Maciel LS, Kochian LV (2018) Emerging pleiotropic mechanisms underlying aluminum resistance and phosphorus acquisition on acidic soils. Front Plant Sci 9:1420. https://doi.org/10.3389/fpls.2018.01420
McBride MB, Zhou Y (2019) Cadmium and zinc bioaccumulation by Phytolacca americana from hydroponic media and contaminated soils. Int J Phytorem 21:1215–1224. https://doi.org/10.1080/15226514.2019.1612849
Meindl GA, Poggioli MI, Bain DJ, Colón MA, Ashman T-L (2021) A test of the inadvertent uptake hypothesis using plant species adapted to serpentine soil. Soil Syst 5:34. https://doi.org/10.3390/soilsystems5020034
Merlot S, García de la Torre VS, Hanikenne M (2021) Physiology and molecular biology of trace element hyperaccumulation. In: van der Ent A, Baker AJM, Echevarria G, Simonnot M-O, Morel JL (eds) Agromining: Farming for Metals, 2nd edn. Mineral Resource Reviews, Springer International Publishing, Cham, pp 155–172
Metali F, Salim KA, Burslem DFRP (2012) Evidence of foliar aluminium accumulation in local, regional and global datasets of wild plants. New Phytol 193:637–649. https://doi.org/10.1111/j.1469-8137.2011.03965.x
Milner MJ, Kochian LV (2008) Investigating heavy-metal hyperaccumulation using Thlaspi caerulescens as a model system. Ann Bot 102:3–13. https://doi.org/10.1093/aob/mcn063
Mizuno T, Hirano K, Hosono A, Kato S, Obata H (2006) Continual pH lowering and manganese dioxide solubilization in the rhizosphere of the Mn-hyperaccumulator plant Chengiopanax sciadophylloides. Soil Sci Plant Nutr 52:726–733. https://doi.org/10.1111/j.1747-0765.2006.00099.x
Nkrumah PN, Navarrete Gutiérrez DM, Tisserand R, van der Ent A, Echevarria G, Pollard AJ, Chaney RL, Morel JL (2021) Element case studies: nickel (tropical regions). In: van der Ent A, Baker AJM, Echevarria G, Simonnot M-O, Morel JL (eds) Agromining: Farming for Metals, 2nd edn. Mineral Resource Reviews, Springer International Publishing, Cham, pp 365–383
Pasricha S, Mathur V, Garg A, Lenka S, Verma K, Agarwal S (2021) Molecular mechanisms underlying heavy metal uptake, translocation and tolerance in hyperaccumulators—an analysis heavy metal tolerance in hyperaccumulators. Environ Chall 4:100197. https://doi.org/10.1016/j.envc.2021.100197
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. https://doi.org/10.1111/j.1420-9101.2006.01178.x
Pollard AJ, Stewart HL, Roberson CB (2009) Manganese hyperaccumulation in Phytolacca americana L. from the southeastern United States. Northeast Nat 16:155–162. https://doi.org/10.1656/045.016.0513
Pollard AJ, Reeves RD, Baker AJM (2014) Facultative hyperaccumulation of heavy metals and metalloids. Plant Sci 217:8–17. https://doi.org/10.1016/j.plantsci.2013.11.011
Puschenreiter M, Wieczorek S, Horak O, Wenzel WW (2003) Chemical changes in the rhizosphere of metal hyperaccumulator and excluder Thlaspi species. J Plant Nutr Soil Sci 166:579–584. https://doi.org/10.1002/jpln.200321155
Reay PF, Waugh C (1981) Mineral-element composition of Lupinus albus and Lupinus angustifolius in relation to manganese accumulation. Plant Soil 60:435–444. https://doi.org/10.1007/BF02149639
Reeves RD (2003) Tropical hyperaccumulators of metals and their potential for phytoextraction. Plant Soil 249:57–65. https://doi.org/10.1023/A:1022572517197
Reeves RD, Baker AJM, Jaffré T, Erskine PD, Echevarria G, van der Ent A (2017) A global database for plants that hyperaccumulate metal and metalloid trace elements. New Phytol 218(2):407–411. https://doi.org/10.1111/nph.14907
Remigo AC, Chaney RL, Baker AJM, Edraki M, Erskine PD, Echevarria G, van der Ent A (2020) Phytoextraction of high value elements and contaminants from mining and mineral wastes: opportunities and limitations. Plant Soil 449:11–37. https://doi.org/10.1007/s11104-020-04487-3
Shan X, Wang H, Zhang S, Zhou H, Zheng Y, Yu H, Wen B (2003) Accumulation and uptake of light rare earth elements in a hyperaccumulator Dicranopteris dichotoma. Plant Sci 165:1343–1353. https://doi.org/10.1016/S0168-9452(03)00361-3
Shane MW, Lambers H (2005) Manganese accumulation in leaves of Hakea prostrata (Proteaceae) and the significance of cluster roots for micronutrient uptake as dependent on phosphorus supply. Physiol Plant 124:441–450. https://doi.org/10.1111/j.1399-3054.2005.00527.x
Skuza L, Szućko-Kociuba I, Filip E, Bożek I (2022) Natural molecular mechanisms of plant hyperaccumulation and hypertolerance towards heavy metals. Int J Mol Sci 23:9335. https://doi.org/10.3390/ijms23169335
Stein RJ, Höreth S, de Melo RF, Syllwasschy L, Lee G, Garbin ML, Clemens S, Krämer U (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. https://doi.org/10.1111/nph.14219
Tao J, Lu L (2022) Advances in genes encoding transporters for cadmium uptake, translocation, and accumulation in plants. Toxics 10:411. https://doi.org/10.3390/toxics10080411
Thomas WA (1975) Accumulation of rare earths and circulation of cerium by mockernut hickory trees. Can J Bot 53:1159–1165. https://doi.org/10.1139/b75-139
Tyler G (2004) Rare earth elements in soil and plant systems – a review. Plant Soil 267:191–206. https://doi.org/10.1007/s11104-005-4888-2
van der Pas L, Ingle RA (2019) Towards an understanding of the molecular basis of nickel hyperaccumulation in plants. Plants 8:11. https://doi.org/10.3390/plants8010011
van der Ent A, Baker AJM, Reeves RD, Pollard AJ, Schat H (2013) Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant Soil 362:319–334. https://doi.org/10.1007/s11104-012-1287-3
van der Ent A, Echevarria G, Tibbett M (2016) Delimiting soil chemistry thresholds for nickel hyperaccumulator plants in Sabah (Malaysia). Chemoecology 26:67–82. https://doi.org/10.1007/s00049-016-0209-x
van der Ent A, Echevarria G, Pollard AJ, Erskine PD (2019a) X-ray fluorescence ionomics of herbarium collections. Sci Rep 9:4746. https://doi.org/10.1038/s41598-019-40050-6
van der Ent A, Ocenar A, Tisserand R, Sugau JB, Erskine PD, Echevarria G (2019b) Herbarium X-ray fluorescence screening for nickel, cobalt and manganese hyperaccumulation in the flora of Sabah (Malaysia, Borneo Island). J Geochem Explor 202:49–58. https://doi.org/10.1016/j.gexplo.2019.03.013
van der Ent A, Pollard AJ, Echevarria G, Abubakari F, Erskine PD, Baker AJM, Reeves RD (2021) Exceptional uptake and accumulation of chemical elements in plants: extending the hyperaccumulation paradigm. In: van der Ent A, Baker AJM, Echevarria G, Simonnot M-O, Morel JL (eds) Agromining: Farming for Metals, 2nd edn. Mineral Resource Reviews, Springer International Publishing, Cham, pp 99–131
Vondráčková S, Száková J, Drábek O, Tejnecký V, Hejcman M, Müllerová V, Tlustoš P (2015) Aluminium uptake and translocation in Al hyperaccumulator Rumex obtusifolius is affected by low-molecular-weight organic acids content and soil pH. PLoS ONE 10:e0123351. https://doi.org/10.1371/journal.pone.0123351
Weber E (2017) Invasive plant species of the world: a reference guide to environmental weeds, 2nd edn. CABI Publishing, Wallingford
Wenzel WW, Bunkowski M, Puschenreiter M, Horak O (2003) Rhizosphere characteristics of indigenously growing nickel hyperaccumulator and excluder plants on serpentine soil. Environ Pollut 123:131–138. https://doi.org/10.1016/S0269-7491(02)00341-X
Wenzel WW, Lombi E, Adriano DC (2004) Root and rhizosphere processes in metal hyperaccumulation and phytoremediation technology. In: Prasad MNV (ed) Heavy metal stress in plants from biomolecules to ecosystems, 2nd edn. Springer, Berlin, pp 313–344
Xue SG, Chen YX, Reeves RD, Baker AJM, Lin Q, Fernando DR (2004) Manganese uptake and accumulation by the hyperaccumulator plant Phytolacca acinosa Roxb. (Phytolaccaceae). Environ Pollut 131:393–399. https://doi.org/10.1016/j.envpol.2004.03.011
Xue SG, Chen YX, Baker AJM, Reeves RD, Xu H, Lin Q (2005) Manganese uptake and accumulation by two populations of Phytolacca acinosa Roxb. (Phytolaccaceae). Water Air Soil Pollut 160:3–14. https://doi.org/10.1007/s11270-005-3349-0
Xue S, Wang J, Zhou X, Liu H, Chen Y (2010) A critical reappraisal of Phytolacca acinosa Roxb. (Phytolaccaceae)—a manganese-hyperaccumulating plant. Acta Ecol Sin 30:335–338. https://doi.org/10.1016/j.chnaes.2010.10.001
Yang QW, Zeng Q, Xiao F, Liu XL, Pan J, He JF, Li ZY (2013) Investigation of manganese tolerance and accumulation of two Mn hyperaccumulators Phytolacca americana L. and Polygonum hydropiper L. in the real Mn-contaminated soils near a manganese mine. Environ Earth Sci 68:1127–1134. https://doi.org/10.1007/s12665-012-1814-9
Yang Z, Yang F, Liu JL, Wu HT, Yang H, Shi Y, Liu J, Zhang YF, Luo YR, Chen KM (2022) Heavy metal transporters: Functional mechanisms, regulation, and application in phytoremediation. Sci Tot Environ 809:151099. https://doi.org/10.1016/j.scitotenv.2021.151099
Ye D, Li T, Liu D, Zhang X, Zheng Z (2015) P accumulation and physiological responses to different high P regimes in Polygonum hydropiper for understanding a P-phytoremediation strategy. Sci Rep 5:17835. https://doi.org/10.1038/srep17835
Yuan M, Tie BQ, Tang MZ, Isao A (2007) Accumulation and uptake of manganese in a hyperaccumulator Phytolacca americana. Miner Engin 20:188–190. https://doi.org/10.1016/j.mineng.2006.06.003
Yuan M, Liu C, Liu WS, Guo MN, Morel JL, Huot H, Yu HJ, Tang YT, Qiu RL (2018) Accumulation and fractionation of rare earth elements (REEs) in the naturally grown Phytolacca americana L. in southern China. Int J Phytorem 20:415–423. https://doi.org/10.1080/15226514.2017.1365336
Zhao FJ, Hamon RE, McLaughlin MJ (2001) Root exudates of the hyperaccumulator Thlaspi caerulescens do not enhance metal mobilization. New Phytol 151:613–620. https://doi.org/10.1046/j.0028-646x.2001.00213.x
Zhao L, Zhu YH, Wang M, Ma LG, Han YG, Zhang MJ, Li XC, Feng WS, Zheng XK (2021) Comparative transcriptome analysis of the hyperaccumulator plant Phytolacca americana in response to cadmium stress. 3 Biotech 11:327. https://doi.org/10.1007/s13205-021-02865-x
Zhou XM, Ranathunge K, Cambridge ML, Dixon KW, Hayes PE, Nikolic M, Shen Q, Zhong H, Lambers H (2022) A cool spot in a biodiversity hotspot: why do tall Eucalyptus forests in southwest Australia exhibit low diversity? Plant Soil 476:669–688. https://doi.org/10.1007/s11104-022-05559-2
Acknowledgements
Many of the ideas expressed in this Commentary stem from years of productive conversations with many colleagues, whose input I gratefully acknowledge.
The author has no relevant financial or non-financial interests to disclose.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Hans Lambers.
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Pollard, A.J. Inadvertent uptake of trace elements and its role in the physiology and evolution of hyperaccumulators. Plant Soil 483, 711–719 (2023). https://doi.org/10.1007/s11104-022-05856-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-022-05856-w