Skip to main content
SpringerLink
Log in

Variation in rare earth element (REE), aluminium (Al) and silicon (Si) accumulation among populations of the hyperaccumulator Dicranopteris linearis in southern China

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Aims

Dicranopteris linearis is a rare earth element (REE), aluminium (Al) and silicon (Si) hyperaccumulator plant which occurs in southern China. To date, there have been no studies on the variation in elemental accumulation among populations of Dicranopteris linearis occurring on REE-enriched and non-REE enriched soils.

Methods

In total 43 Dicranopteris linearis individuals and the corresponding rhizosphere soils from 7 populations in southern China were sampled and the plant material and soil composition were chemically analysed for REE and other elements.

Results

Dicranopteris linearis populations from REE-enriched soils and non-REE enriched soils both have the ability to accumulate high concentrations of REE (> 1000 mg kg− 1), Al (> 1000 mg kg− 1) and Si (> 10 000 mg kg− 1). The ratios of light REEs (LREEs) to heavy REEs (HREEs) in Dicranopteris linearis pinnae are consistently > 1, regardless of their ratios in the corresponding soils. Concentrations of REE in Dicranopteris linearis pinnae vary significantly among populations and have positive correlations with total and extractable soil REE concentrations. The plant Al and Si concentrations in Dicranopteris linearis populations are uncoupled from variations in soil Al and Si concentrations. The plant REE concentrations have no obvious relationships with the prevailing Al concentrations, but are positively correlated with plant Si and Mn, and negatively correlated with soil extractable P concentrations.

Conclusions

The hyperaccumulation of REEs (LREE > HREE), Al and Si in non-REE enriched soils is a species-wide trait. The accumulation of REEs is highly variable and associated with soil REE concentrations, nutrients status, and other soil properties.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Adamidis GC, Dimitrakopoulos PG, Manolis A, Papageorgiou AC (2014) Genetic diversity and population structure of the serpentine endemic Ni hyperaccumulator Alyssum lesbiacum. Plant Syst Evol 300:2051–2060

    Article  Google Scholar 

  • Assunção AGL, Bleeker P, Bookum WM, Vooijs R, Schat H (2008) Intraspecific variation of metal preference patterns for hyperaccumulation in Thlaspi caerulescens: Evidence from binary metal exposures. Plant Soil 303:289–299

    Article  CAS  Google Scholar 

  • Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements: A review of their distribution, ecology and phytochemistry. Biorecovery 1:81–126

    CAS  Google Scholar 

  • Baker AJM, Proctor J (1990) The influence of cadmium, copper, lead, and zinc on the distribution and evolution of metallophytes in the British isles. Plant Syst Evol 173:91–108

    Article  CAS  Google Scholar 

  • Bert V, Bonnin I, Saumitou-Laprade P, de Laguérie P, Petit D (2002) Do Arabidopsis halleri from nonmetallicolous populations accumulate zinc and cadmium more effectively than those from metallicolous populations? New Phytol 155:47–57

    Article  CAS  PubMed  Google Scholar 

  • Boyd (2004) Ecology of metal hyperaccumulation. New Phytol 162:563–567

    Article  PubMed  Google Scholar 

  • Brioschi L, Steinmann M, Lucot E, Pierret MC, Stille P, Prunier J, Badot PM (2013) Transfer of rare earth elements (REE) from natural soil to plant systems: Implications for the environmental availability of anthropogenic REE. Plant Soil 366:143–163

    Article  CAS  Google Scholar 

  • Chaney RL, Angle JS, Broadhurst CL, Peters CA, Tappero RV, Sparks DL (2007) Improved understanding of hyperaccumulation yields commercial phytoextraction and phytomining technologies. J Environ Qual 36:1429–1443

    Article  CAS  PubMed  Google Scholar 

  • Chardot V, Echevarria G, Gury M, Massoura S, Morel JL (2007) Nickel bioavailability in an ultramafic toposequence in the Vosges mountains (France). Plant Soil 293:7–21

    Article  CAS  Google Scholar 

  • Chen J, Zhong ZC (1991) Characteristics of nutrient elements cycling in fern community. Acta Ecol Sin 11:209–306 (in Chinese)

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Chour Z, Laubie B, Morel JL, Tang YT, Qiu RL, Simonnot MO, Muhr L (2018) Recovery of rare earth elements from Dicranopteris dichotoma by an enhanced ion exchange leaching process. Chem Eng Process 130:208–213

    Article  CAS  Google Scholar 

  • Corzo Remigio A, Edraki M, Erskine PD, Echevarria G, Chaney RL, van der Ent A (2020) Phyto-extraction of high-value elements and contaminants from minerals wastes: Opportunities and limitations. Plant Soil 449(1):11–37

    Article  CAS  Google Scholar 

  • Dechamps C, Roosens NH, Céline Hotte, Meerts P (2005) Growth and mineral element composition in two ecotypes of Thlaspi caerulescens on Cd contaminated soil. Plant Soil 273:327–335

    Article  CAS  Google Scholar 

  • Ding SM, Liang T, Zhang C, Huang Z, Xie Y, Chen T (2006) Fractionation mechanisms of rare earth elements (REEs) in hydroponic wheat: An application for metal accumulation by plants. Environ Sci Technol 40:2686–2691

    Article  CAS  PubMed  Google Scholar 

  • Fung KF, Carr HP, Zhang J, Wong MH (2008) Growth and nutrient uptake of tea under different aluminium concentrations. J Sci Food Agr 15:1582–1591

    Article  CAS  Google Scholar 

  • Groenenberg JE, Römkens PFAM, Comans RNJ, Luster J, Pampura T, Shotbolt L, Tipping E, De Vries W (2010) Transfer functions for solid solution partitioning of cadmium, copper, nickel, lead and zinc in soils: Derivation of relations for free metal ion activities and validation on independent data. Eur J Soil Sci 61:58–73

    Article  CAS  Google Scholar 

  • Han F, Shan XQ, Zhang J, Xie YN, Pei ZG, Zhang SZ, Zhu YG, Wen B (2005) Organic acids promote the uptake of lanthanum by barley roots. New Phytol 165:481–492

    Article  CAS  PubMed  Google Scholar 

  • Hodson MJ, Evans DE (2020) Aluminium–silicon interactions in higher plants: An update. J Exp Bot. https://doi.org/10.1093/jxb/eraa024

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

  • Jordens A, Cheng YP, Waters KE (2013) A review of the beneficiation of rare earth element bearing minerals. Miner Eng 41:97–114

    Article  CAS  Google Scholar 

  • Kameník J, Mizera J, Řanda Z (2013) Chemical composition of plant silica phytoliths. Environ Chem Lett 11:189–195

    Article  CAS  Google Scholar 

  • Khairil M, Burslem DF (2018) Controls on foliar aluminium accumulation among populations of the tropical shrub Melastoma malabathricum L. (Melastomataceae). Tree Physiol 38:1752–1760

    CAS  PubMed  Google Scholar 

  • Lambers H, Hayes PE, Laliberte E, Oliveira RS, Turner BL (2015) Leaf manganese accumulation and phosphorus-acquisition efficiency. Trends Plant Sci 20:83–90

    Article  CAS  Google Scholar 

  • Li QF, Mao ZW, Zhu YW, Huo DW, Zhao HZ, Yi XL, Zhao GW (1992) Research on rare earth elements concentrations in Dicranopteris linearis. Rare Earth 13:16–19 (in Chinese)

    Google Scholar 

  • Li JT, Gurajala HK, Wu LH, van der Ent A, Qiu RL, Baker AJ, Tang YT, Yang XE, Shu WS (2018) Hyperaccumulator plants from China: A synthesis of the current state of knowledge. Environ Sci Technol 52:11980–11994

    Article  CAS  PubMed  Google Scholar 

  • Liang T, Ding SM, Song WC, Chong ZY, Zhang CZ, Li HT (2008) A review of fractionations of rare earth elements in plants. J Rare Earth 26:7–15

    Article  Google Scholar 

  • Liu WS, Liu C, Wang ZW, Teng WK, Tang YT, Qiu RL (2015) Limiting factors for restoration of dumping sites of ionic rare earth mine tailings. Acta Pedol Sin 52:179–187 (in Chinese)

    Google Scholar 

  • Liu C, Yuan M, Liu WS, Guo MN, Huot H, Tang YT, Laubie B, Simonnot MO, Morel JL, Qiu RL (2018) Element case studies: Rare earth elements. In: van der Ent A, Echevarria G, Baker A, Morel JL (eds) Agromining: Farming for metals. Mineral Resource Reviews, Springer, pp 297–308

    Chapter  Google Scholar 

  • Liu WS, Zheng HX, Guo MN, Liu C, Huot H, Morel JL, van der Ent A, Tang YT, Qiu RL (2019a) Co-deposition of silicon with rare earth elements (REEs) and aluminium in the fern Dicranopteris linearis from China. Plant Soil 437:427–437

    Article  CAS  Google Scholar 

  • Liu WS, Guo MN, Liu C, Yuan M, Chen XT, Huot H, Zhao CM, Tang YT, Morel JL, Qiu RL (2019b) Water, sediment and agricultural soil contamination from an ion-adsorption rare earth mining area. Chemosphere 216:75–83

    Article  CAS  PubMed  Google Scholar 

  • Liu WS, van der Ent A, Erskine PD, Morel JL, Echevarria G, Montargès-Pelletier E, Spiers KM, Qiu RL, Tang YT (2020a) Spatially-resolved localization of lanthanum and cerium in the rare earth element hyperaccumulator fern Dicranopteris linearis from China. Environ Sci Technol 54:2287–2294

    Article  CAS  PubMed  Google Scholar 

  • Liu WS, Chen YY, Hermine H, Liu C, Guo MN, Qiu RL, Morel JL, Tang YT (2020b) Phytoextraction of rare earth elements from ion-adsorption mine tailings by Phytolacca americana: Effects of organic material and biochar amendment. J Clean Prod 275:122959

    Article  CAS  Google Scholar 

  • Ma JF, Yamaji N (2006) Silicon uptake and accumulation in higher plants. Trends Plant Sci 11:392–397

    Article  CAS  PubMed  Google Scholar 

  • Metali F, Salim KA, Tennakoon K, Burslem DFRP (2015) Controls on foliar nutrient and aluminium concentrations in a tropical tree flora: Phylogeny, soil chemistry and interactions among elements. New Phytol 205:280–292

    Article  CAS  PubMed  Google Scholar 

  • Neugebauer K, Broadley MR, El, Serehy HA, George TS, McNicol JW, Moraes MF, White PJ (2018) Variation in the angiosperm ionome. Physiol Plant 163:306–322

    Article  CAS  Google Scholar 

  • Pletnev IV, Zernov VV (2002) Classification of metal ions according to their complexing properties: A data-driven approach. Analyt Chim Acta 455:131–142

    Article  CAS  Google Scholar 

  • Pollard AJ, Powell KD, Harper FA, Smith JAC (2002) The genetic basis of metal hyperaccumulation in plants. Crit Rev Plant Sci 21:539–566

    Article  CAS  Google Scholar 

  • Pollard AJ, Reeves RD, Baker AJM (2014) Facultative hyperaccumulation of heavy metals and metalloids. Plant Sci 217–218:8–17

    Article  PubMed  CAS  Google Scholar 

  • Pryer KM, Schneider H, Smith AR, Cranfill R, Wolf PG, Hunt JS, Sipes SD (2001) Horsetails and ferns are a monophyletic group and the closest living relatives to seed plants. Nature 409:618

    Article  CAS  PubMed  Google Scholar 

  • Raven JA (2003) Cycling silicon–the role of accumulation in plants. New Phytol 158:419–421

    Article  Google Scholar 

  • Reeves RD (2006) Hyperaccumulation of trace elements by plants. In: Morel JL, Echevarria G, Goncharova N (eds) Phytoremediation of metal-contaminated soils, vol 68. Springer, Dordrecht NATO Science Series

  • Roosens NH, Verbruggen N, Meerts P, Ximénez-Embún P, Smith JAC (2003) Natural variation in cadmium tolerance and its relationship to metal hyperaccumulation for seven populations of Thlaspi caerulescens from western Europe. Plant Cell Environ 26:1657–1672

    Article  CAS  Google Scholar 

  • Russell AE, Raich JW, Vitousek PM (1998) The ecology of the climbing fern Dicranopteris linearis, on windward Mauna Loa, Hawaii. J Ecol 86:765–779

    Article  Google Scholar 

  • Russell AE, Hall SJ, Raich JW (2017) Tropical tree species traits drive soil cation dynamics via effects on pH: A proposed conceptual framework. Ecol Monogr 87:685–701

    Article  Google Scholar 

  • Schmitt M, Mehltreter K, Sundue M, Testo W, Watanabe T, Jansen S (2017) The evolution of aluminum accumulation in ferns and lycophytes. Am J Bot 104:573–583

    Article  CAS  PubMed  Google Scholar 

  • Shan XQ, Wang H, Zhang S, Zhou H, Zheng Y, Yu H, Wen B (2003) Accumulation and uptake of light rare earth elements in a hyperaccumulator Dicropteris dichotoma. Plant Sci 165:1343–1353

    Article  CAS  Google Scholar 

  • Stein RJ, Höreth S, de Melo JRF, Syllwasschy L, Lee G, Garbin ML, Clemens S, Kramer U (2017) Relationships between soil and leaf mineral composition are element-specific, environment-dependent and geographically structured in the emerging model Arabidopsis helleri. New Phytol 213:1274–1286

    Article  CAS  PubMed  Google Scholar 

  • Tang YT, Cloquet C, Deng THB, Sterckeman T, Echevarria G, Yang WJ, Morel MJ, Qiu RL (2016) Zinc isotope fractionation in the hyperaccumulator Noccaea caerulescens and the nonaccumulating plant Thlaspi arvense at low and high Zn supply. Environ Sci Technol 50:8020–8027

    Article  CAS  PubMed  Google Scholar 

  • Tyler G (2004) Rare earth elements in soil and plant systems-A review. Plant Soil 267(1–2):191–206

    Article  CAS  Google Scholar 

  • USDA (2018) Agricultural Research Service, National Plant Germplasm System. Germplasm Resources Information Network (GRIN-Taxonomy)

  • 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

    Article  CAS  Google Scholar 

  • van der Ent A, Baker AJM, Reeves RD, Chaney RL, Anderson CWN, Meech JA, Erskine PD, Simonnot MO, Vaughan J, Morel JL, Echevarria G, Fogliani B, Qiu QL, Mulligan DR (2015) Agromining: Farming for metals in the future? Environ Sci Technol 49:4773–4780

    Article  PubMed  CAS  Google Scholar 

  • Wang LF, Ji HB, Bai KZ, Li LB, Kuang TY (2006) Photosystem 2 activities of hyper-accumulator Dicranopteris dichotoma Bernh from a light rare earth elements mine. Photosynthetica 44:202–207

    Article  CAS  Google Scholar 

  • Wei ZG, Yin M, Zhang X, Hong FS, Li B, Tao Y, Zhao GW, Yan CH (2001) Rare earth elements in naturally grown fern Dicranopteris linearis in relation to their variation in soils in South-Jiangxi region (Southern China). Environ Pollut 114:345–355

    Article  CAS  PubMed  Google Scholar 

  • Wei ZG, Hong FS, Yin M, Li HX, Hu F, Zhao GW, Wong JWC (2004) Off-line separation and determination of rare earth elements associated with chloroplast pigments of hyperaccumulator Dicranopteris dichotoma by normal-phase liquid chromatography and ICP–MS. Analyt Bioanal Chem 380:677–682

    Article  CAS  Google Scholar 

  • Wei ZG, Hong FS, Yin M, Li HX, Hu F, Zhao GW, Wong JWC (2005) Subcellular and molecular localization of rare earth elements and structural characterization of yttrium bound chlorophyll a in naturally grown fern Dicranopteris dichotoma. Microchem J 80:1–8

    Article  CAS  Google Scholar 

  • Wei ZG, Zhang HJ, Li HX, Hu F (2006) Research trends on rare earth Element hyperaccumulator. J Chinese Rare Earth Soc 24:1–11 (in Chinese)

    CAS  Google Scholar 

  • Yuan M, Guo MN, Liu WS, Liu C, van der Ent A, Morel JL, Huot H, Zhao WY, Wei XG, Qiu RL, Tang YT (2017) The accumulation and fractionation of rare earth elements in hydroponically grown Phytolacca americana L. Plant Soil 421:67–82

    Article  CAS  Google Scholar 

  • Zhang P, Ma YH, Zhang ZY, He X, Guo Z, Tai RZ, Ding YY, Zhao YL, Chai ZF (2012) Comparative toxicity of nanoparticulate/bulk Yb2O3 and YbCl3 to cucumber (Cucumis sativus). Environ Sci Technol 46:1834–1841

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (NSFC) [Grant No. 41771343], and the Key R&D Program of Jiangxi Province [Grant No. 20192ACB70016]. This work is a contribution of the joint lab ECOLAND, established between Sun Yat-sen University and the University of Lorraine and INRAE.

Author information

Authors and Affiliations

  1. School of Environmental Science and Engineering, Guangdong Provincial Key Laboratory of Environmental Pollution Control and Remediation Technology, Guangdong Provincial Engineering Research Center for Heavy Metal Contaminated Soil Remediation, Sun Yat-sen University, 510275, Guangzhou, China

    Wen-Shen Liu, Hong-Xiang Zheng, Chang Liu, Mei-Na Guo, Shi-Chen Zhu, Yue Cao, Rong-Liang Qiu & Ye-Tao Tang

  2. Guangdong Laboratory for Lingnan Modern Agriculture, South China Agriculture University, 510642, Guangzhou, China

    Rong-Liang Qiu

  3. Laboratoire Sols et Environnement, Université de Lorraine, INRAE, 54518, Vandoeuvre-lès-Nancy, France

    Jean Louis Morel

  4. Centre for Mined Land Rehabilitation, Sustainable Minerals Institute, The University of Queensland, St Lucia, Queensland, 4072, Australia

    Antony van der Ent

Authors
  1. Wen-Shen Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hong-Xiang Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mei-Na Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shi-Chen Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yue Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Rong-Liang Qiu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jean Louis Morel
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Antony van der Ent
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Ye-Tao Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ye-Tao Tang.

Additional information

Responsible Editor: Juan Barcelo.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

ESM 1

(DOCX 461 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, WS., Zheng, HX., Liu, C. et al. Variation in rare earth element (REE), aluminium (Al) and silicon (Si) accumulation among populations of the hyperaccumulator Dicranopteris linearis in southern China. Plant Soil 461, 565–578 (2021). https://doi.org/10.1007/s11104-021-04835-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-021-04835-x

Keywords

Search

Navigation