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Environmental problems - Chemical approaches
RESEARCH ARTICLE

Identification of new hardy ferns that preferentially accumulate light rare earth elements: a conserved trait within fern species

Nicolas Grosjean A B , Damien Blaudez https://orcid.org/0000-0003-3287-3482 B , Michel Chalot C D , Elisabeth Maria Gross A and Marie Le Jean https://orcid.org/0000-0001-5470-4749 A E
+ Author Affiliations
- Author Affiliations

A Université de Lorraine, CNRS, LIEC, F-57000 Metz, France.

B Université de Lorraine, CNRS, LIEC, F-54000 Nancy, France.

C Université de Bourgogne Franche-Comté, CNRS, Laboratoire Chrono-environnement, F-25211, Montbéliard, France.

D Université de Lorraine, F-54000 Nancy, France.

E Corresponding author. Email: marie.lejean@univ-lorraine.fr

Environmental Chemistry 17(2) 191-200 https://doi.org/10.1071/EN19182
Submitted: 20 June 2019  Accepted: 21 September 2019   Published: 6 November 2019

Environmental context. Rare earth elements (REEs) are strategic metals and emerging contaminants for which plant-based remediation measures are needed. We screened a collection of hardy ferns and identified new accumulator species that preferentially transferred light REEs to their fronds. This study is an important step towards understanding the mechanisms of REE accumulation in plants.

Abstract. Rare earth elements (REEs) include the lanthanides plus yttrium and scandium, and can be split according to their atomic mass into light (LREEs) and heavy REEs (HREEs). The increasing demand for REEs is mainly driven by new technologies, and their current low recyclability has led them to become emerging contaminants. The identification of new REE accumulators may help in determining the REE transfer mechanisms and may result in interesting candidates for phytoremediation techniques. To that end, a collection of 49 hardy fern species, grown in REE-spiked substrate, were screened for their potential in REE accumulation. REE concentrations were very low in the fronds of all Polypodium species, whereas all Athyrium species highly accumulated REEs. The REE accumulation level was more variable among the different species of Dryopteris, Blechnum, Woodwardia, Cystopteris and Polystichum. However, whatever the species, LREEs were preferentially transferred to the fronds over HREEs. This conserved trait was independent of the availability of different REEs in the substrate and instead may arise from specific transfer systems in ferns for the two groups of REEs. Furthermore, REE accumulation was correlated to Ca and Al, which suggested the existence of common uptake pathways. Altogether, these results are of great interest for phytoremediation purposes since appropriate species can be chosen according to the area to be remediated, and they also provide new insights into a more in-depth characterisation of the underlying REE accumulation mechanisms in ferns.

Additional keywords: Dryopteris, lanthanides, REE-accumulation, REE-fractionation, yttrium.


References

Binnemans K, Jones PT, Blanpain B, Van Gerven T, Yang Y, Walton A, Buchert M (2013). Recycling of rare earths: A critical review. Journal of Cleaner Production 51, 1–22.
Recycling of rare earths: A critical reviewCrossref | GoogleScholarGoogle 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 and Soil 366, 143–163.
Transfer of rare earth elements (REE) from natural soil to plant systems: implications for the environmental availability of anthropogenic REECrossref | GoogleScholarGoogle Scholar |

Cantrell KJ, Byrne RH (1987). Rare earth element complexation by carbonate and oxalate ions. Geochimica et Cosmochimica Acta 51, 597–605.
Rare earth element complexation by carbonate and oxalate ionsCrossref | GoogleScholarGoogle Scholar |

Chaney RL, Malik M, Li YM, Brown SL, Brewer EP, Angle JS, Baker AJ (1997). Phytoremediation of soil metals. Current Opinion in Biotechnology 8, 279–284.
Phytoremediation of soil metalsCrossref | GoogleScholarGoogle Scholar | 9206007PubMed |

Cheisson T, Schelter EJ (2019). Rare earth elements: Mendeleev’s bane, modern marvels. Science 363, 489–493.
Rare earth elements: Mendeleev’s bane, modern marvelsCrossref | GoogleScholarGoogle Scholar | 30705185PubMed |

Ciacci L, Reck BK, Nassar NT, Graedel TE (2015). Lost by design. Environmental Science & Technology 49, 9443–9451.
Lost by designCrossref | GoogleScholarGoogle Scholar |

Cotton S (2006). ‘Lanthanide and actinide chemistry.’ (John Wiley: Hoboken, NJ)

Deng B, Du W, Liu C, Sun W, Tian S, Dong H (2012). Antioxidant response to drought, cold and nutrient stress in two ploidy levels of tobacco plants: low resource requirement confers polytolerance in polyploids?. Plant Growth Regulation 66, 37–47.
Antioxidant response to drought, cold and nutrient stress in two ploidy levels of tobacco plants: low resource requirement confers polytolerance in polyploids?Crossref | GoogleScholarGoogle Scholar |

Ding SM, Liang T, Zhang CS, Yan JC, Zhang ZL (2005). Accumulation and fractionation of rare earth elements (REEs) in wheat: Controlled by phosphate precipitation, cell wall absorption and solution complexation. Journal of Experimental Botany 56, 2765–2775.
Accumulation and fractionation of rare earth elements (REEs) in wheat: Controlled by phosphate precipitation, cell wall absorption and solution complexationCrossref | GoogleScholarGoogle Scholar |

Ding S, 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. Environmental Science & Technology 40, 2686–2691.
Fractionation mechanisms of rare earth elements (REEs) in hydroponic wheat: an application for metal accumulation by plantsCrossref | GoogleScholarGoogle Scholar |

Ding SM, Liang T, Yan JC, Zhang ZL, Huang ZC, Xie YN (2007). Fractionations of rare earth elements in plants and their conceptive model. Science in China. Series C, Life Sciences 50, 47–55.
Fractionations of rare earth elements in plants and their conceptive modelCrossref | GoogleScholarGoogle Scholar |

Djingova R, Ivanova J, Wagner G, Korhammer S, Markert B (2001). Distribution of lanthanoids, Be, Bi, Ga, Te, Tl, Th and U on the territory of Bulgaria using Populus nigra ‘Italica’ as an indicator. The Science of the Total Environment 280, 85–91.
Distribution of lanthanoids, Be, Bi, Ga, Te, Tl, Th and U on the territory of Bulgaria using Populus nigra ‘Italica’ as an indicatorCrossref | GoogleScholarGoogle Scholar | 11763275PubMed |

Fageria NK, Baligar VC, Clark RB (2004). ‘Micronutrients in crop production: advances in agronomy.’ (Elsevier Inc.: Amsterdam)

Gambogi J (2018). Rare earths. U.S. Geological Survey Minerals Yearbook 2015, Vol. 1 – Metals and Minerals.

Gonzalez V, Vignati DAL, Leyval C, Giamberini L (2014). Environmental fate and ecotoxicity of lanthanides: Are they a uniform group beyond chemistry?. Environment International 71, 148–157.
Environmental fate and ecotoxicity of lanthanides: Are they a uniform group beyond chemistry?Crossref | GoogleScholarGoogle Scholar | 25036616PubMed |

Hedrick JB (2003). Rare earths. U.S. Geological Survey Minerals Yearbook 2001, Vol. 1 – Metals and Minerals.

Hori K, Watano Y, Murakami N (2016). Hybrid origin of the apogamous fern Dryopteris hondoensis (Dryopteridaceae). Acta Phytotaxonomica et Geobotanica 67, 133–146.
Hybrid origin of the apogamous fern Dryopteris hondoensis (Dryopteridaceae)Crossref | GoogleScholarGoogle Scholar |

Ichihashi H, Morita H, Tatsukawa R (1992). Rare earth elements (REEs) in naturally grown plants in relation to their variation in soils. Environmental Pollution 76, 157–162.
Rare earth elements (REEs) in naturally grown plants in relation to their variation in soilsCrossref | GoogleScholarGoogle Scholar | 15091997PubMed |

Ikhlayel M (2017). Evaluation of the environmental impacts of rare earth elements production. International Journal of Environmental Studies 74, 939–957.
Evaluation of the environmental impacts of rare earth elements productionCrossref | GoogleScholarGoogle Scholar |

Jelusic M, Lestan D (2015). Remediation and reclamation of soils heavily contaminated with toxic metals as a substrate for greening with ornamental plants and grasses. Chemosphere 138, 1001–1007.
Remediation and reclamation of soils heavily contaminated with toxic metals as a substrate for greening with ornamental plants and grassesCrossref | GoogleScholarGoogle Scholar | 25577699PubMed |

Krämer U (2010). Metal hyperaccumulation in plants. Annual Review of Plant Biology 61, 517–534.
Metal hyperaccumulation in plantsCrossref | GoogleScholarGoogle Scholar | 20192749PubMed |

Lai Y, Wang QQ, Yan WW, Yang LM, Huang BL (2005). Preliminary study of the enrichment and fractionation of REEs in a newly discovered REE hyperaccumulator Pronephrium simplex by SEC-ICP-MS and MALDI-TOF/ESI-MS. Journal of Analytical Atomic Spectrometry 20, 751–753.
Preliminary study of the enrichment and fractionation of REEs in a newly discovered REE hyperaccumulator Pronephrium simplex by SEC-ICP-MS and MALDI-TOF/ESI-MSCrossref | GoogleScholarGoogle Scholar |

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.
Subcellular distribution of rare earth elements and characterization of their binding species in a newly discovered hyperaccumulator Pronephrium simplexCrossref | GoogleScholarGoogle Scholar | 18970723PubMed |

Liang T, Ding S, Song W, Chong Z, Zhang C, Li H (2008). A review of fractionations of rare earth elements in plants. Journal of Rare Earths 26, 7–15.
A review of fractionations of rare earth elements in plantsCrossref | GoogleScholarGoogle Scholar |

Liang T, Li K, Wang L (2014). State of rare earth elements in different environmental components in mining areas of China. Environmental Monitoring and Assessment 186, 1499–1513.
State of rare earth elements in different environmental components in mining areas of ChinaCrossref | GoogleScholarGoogle Scholar | 24135922PubMed |

Liu JN, Zhou QX, Sun T, Ma LQ, Wang S (2008). Growth responses of three ornamental plants to Cd and Cd-Pb stress and their metal accumulation characteristics. Journal of Hazardous Materials 151, 261–267.
Growth responses of three ornamental plants to Cd and Cd-Pb stress and their metal accumulation characteristicsCrossref | GoogleScholarGoogle Scholar | 17869419PubMed |

Liu C, Yuan M, Liu W, Guo M, Huot H, Tang Y, Laubie B, Simonnot M, Morel J, Qiu R (2017). Element case studies: rare earth elements. In ‘Agromining: Farming for metals’. (Eds A Van der Ent, G Echevarria, A Baker, JL Morel) pp. 297–308 (Springer: Cham)

Long KR, Van Gosen BS, Foley NK, Cordier D (2010). The principal rare earth elements deposits of the United States: A summary of domestic deposits and a global perspective. U.S. Geological Survey Scientific Investigations Report 2010–5220. Available at http://pubs.usgs.gov/sir/2010/5220/ [verified 3 October 2019]

Ozaki T, Enomoto S, Minai Y, Ambe S, Ambe F, Tominaga T (1997). Determination of lanthanides and other trace elements in ferns by instrumental neutron activation analysis. Journal of Radioanalytical and Nuclear Chemistry 217, 117–124.
Determination of lanthanides and other trace elements in ferns by instrumental neutron activation analysisCrossref | GoogleScholarGoogle Scholar |

Ozaki T, Enomoto S, Minai Y, Ambe S, Ambe F, Makide Y (2000). Beneficial effect of rare earth elements on the growth of Dryopteris erythrosora. Journal of Plant Physiology 156, 330–334.
Beneficial effect of rare earth elements on the growth of Dryopteris erythrosoraCrossref | GoogleScholarGoogle Scholar |

Padmavathiamma PK, Li LY (2007). Phytoremediation technology: Hyper-accumulation metals in plants. Water, Air, and Soil Pollution 184, 105–126.
Phytoremediation technology: Hyper-accumulation metals in plantsCrossref | GoogleScholarGoogle Scholar |

Pagano G, Guida M, Tommasi F, Oral R (2015). Health effects and toxicity mechanisms of rare earth elements – Knowledge gaps and research prospects. Ecotoxicology and Environmental Safety 115, 40–48.
Health effects and toxicity mechanisms of rare earth elements – Knowledge gaps and research prospectsCrossref | GoogleScholarGoogle Scholar | 25679485PubMed |

Pittermann J, Limm E, Rico C, Christman MA (2011). Structure-function constraints of tracheid-based xylem: A comparison of conifers and ferns. New Phytologist 192, 449–461.
Structure-function constraints of tracheid-based xylem: A comparison of conifers and fernsCrossref | GoogleScholarGoogle Scholar | 21749396PubMed |

Ramos SJ, Dinali GS, de Carvalho TS, Chaves LC, Siqueira JO, Guilherme LRG (2016). Rare earth elements in raw materials and products of the phosphate fertilizer industry in South America: Content, signature, and crystalline phases. Journal of Geochemical Exploration 168, 177–186.
Rare earth elements in raw materials and products of the phosphate fertilizer industry in South America: Content, signature, and crystalline phasesCrossref | GoogleScholarGoogle Scholar |

Rengel Z, Marschner P (2005). Nutrient availability and management in the rhizosphere: Exploiting genotypic differences. New Phytologist 168, 305–312.
Nutrient availability and management in the rhizosphere: Exploiting genotypic differencesCrossref | GoogleScholarGoogle Scholar | 16219070PubMed |

Rim KT, Koo KH, Park JS (2013). Toxicological evaluations of rare earths and their health impacts to workers: a literature review. Safety and Health at Work 4, 12–26.
Toxicological evaluations of rare earths and their health impacts to workers: a literature reviewCrossref | GoogleScholarGoogle Scholar | 23516020PubMed |

Salazar MJ, Pignata ML (2014). Lead accumulation in plants grown in polluted soils. Screening of native species for phytoremediation. Journal of Geochemical Exploration 137, 29–36.
Lead accumulation in plants grown in polluted soils. Screening of native species for phytoremediationCrossref | GoogleScholarGoogle Scholar |

Sessa EB, Zimmer EA, Givnish TJ (2012). Unraveling reticulate evolution in North American Dryopteris (Dryopteridaceae). BMC Evolutionary Biology 12, 104
Unraveling reticulate evolution in North American Dryopteris (Dryopteridaceae)Crossref | GoogleScholarGoogle Scholar | 22748145PubMed |

Shahandeh H, Hossner LR (2000). Plant screening for chromium phytoremediation. International Journal of Phytoremediation 2, 31–51.
Plant screening for chromium phytoremediationCrossref | GoogleScholarGoogle Scholar |

Shan XQ, Lian J, Wen B (2002). Effect of organic acids on adsorption and desorption of rare earth elements. Chemosphere 47, 701–710.
Effect of organic acids on adsorption and desorption of rare earth elementsCrossref | GoogleScholarGoogle Scholar | 12079065PubMed |

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 Dicropteris dichotoma. Plant Science 165, 1343–1353.
Accumulation and uptake of light rare earth elements in a hyperaccumulator Dicropteris dichotomaCrossref | GoogleScholarGoogle Scholar |

Suzuki Y, Yokoi S, Katoh M, Minato M, Takizawa N (1980). Stability constants of rare-earth complexes with some organic ligands. In ‘The rare earths in modern science and technology’. (Eds GJ McCarthy, JJ Rhyne, HB Silber) pp. 121–126. (Springer: Boston, MA)

Tyler G (2004). Rare earth elements in soil and plant systems – A review. Plant and Soil 267, 191–206.
Rare earth elements in soil and plant systems – A reviewCrossref | GoogleScholarGoogle Scholar |

Visioli G, D’Egidio S, Sanangelantoni AM (2015). The bacterial rhizobiome of hyperaccumulators: future perspectives based on omics analysis and advanced microscopy. Frontiers in Plant Science 5, 752
The bacterial rhizobiome of hyperaccumulators: future perspectives based on omics analysis and advanced microscopyCrossref | GoogleScholarGoogle Scholar | 25709609PubMed |

Wakabayashi T, Ymamoto A, Kazaana A, Nakano Y, Nojiri Y, Kashiwazaki M (2016). Antibacterial, antifungal and nematicidal activities of rare earth ions. Biological Trace Element Research 174, 464–470.
Antibacterial, antifungal and nematicidal activities of rare earth ionsCrossref | GoogleScholarGoogle Scholar | 27147430PubMed |

Wang H, Shan X-Q, Zhang S, Wen B (2003). Preliminary characterization of a light-rare-earth-element-binding peptide of a natural perennial fern Dicranopteris dichotoma. Analytical and Bioanalytical Chemistry 376, 49–52.
Preliminary characterization of a light-rare-earth-element-binding peptide of a natural perennial fern Dicranopteris dichotomaCrossref | GoogleScholarGoogle Scholar | 12734617PubMed |

Wang LF, Ji HB, Bai KZ, Li LB, Kuang TY (2005). Photosynthetic characterization of the plant Dicranopteris dichotoma Bernh. in a rare earth elements mine. Journal of Integrative Plant Biology 47, 1092–1100.
Photosynthetic characterization of the plant Dicranopteris dichotoma Bernh. in a rare earth elements mineCrossref | GoogleScholarGoogle Scholar |

Wei Z, Yin M, Zhang X, Hong F, Li B, Tao Y, Zhao G, Yan C (2001). Rare earth elements in naturally grown fern Dicranopteris linearis in relation to their variation in soils in South-Jiangxi region (Southern China). Environmental Pollution 114, 345–355.
Rare earth elements in naturally grown fern Dicranopteris linearis in relation to their variation in soils in South-Jiangxi region (Southern China)Crossref | GoogleScholarGoogle Scholar | 11584633PubMed |

Wiche O, Kummer NA, Heilmeier H (2016). Interspecific root interactions between white lupin and barley enhance the uptake of rare earth elements (REEs) and nutrients in shoots of barley. Plant and Soil 402, 235–245.
Interspecific root interactions between white lupin and barley enhance the uptake of rare earth elements (REEs) and nutrients in shoots of barleyCrossref | GoogleScholarGoogle Scholar |

Wood BW, Grauke LJ (2011). The rare-earth metallome of pecan and other Carya. Journal of the American Society for Horticultural Science 136, 389–398.
The rare-earth metallome of pecan and other CaryaCrossref | GoogleScholarGoogle Scholar |

Wu JL, Wei ZG, Zhao HY, Li HX, Hu F (2009). The role of amino acids in the long-distance transport of La and Y in the xylem sap of tomato. Biological Trace Element Research 129, 239–250.
The role of amino acids in the long-distance transport of La and Y in the xylem sap of tomatoCrossref | GoogleScholarGoogle Scholar | 19048192PubMed |

Wu J, Chen A, Peng S, Wei Z, Liu G (2013). Identification and application of amino acids as chelators in phytoremediation of rare earth elements lanthanum and yttrium. Plant and Soil 373, 329–338.
Identification and application of amino acids as chelators in phytoremediation of rare earth elements lanthanum and yttriumCrossref | GoogleScholarGoogle Scholar |

Wu M, Luo Q, Liu S, Zhao Y, Long Y, Pan Y (2018). Screening ornamental plants to identify potential Cd hyperaccumulators for bioremediation. Ecotoxicology and Environmental Safety 162, 35–41.
Screening ornamental plants to identify potential Cd hyperaccumulators for bioremediationCrossref | GoogleScholarGoogle Scholar | 29960120PubMed |

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 and Soil 421, 67–82.
The accumulation and fractionation of rare earth elements in hydroponically grown Phytolacca americana LCrossref | GoogleScholarGoogle Scholar |

Yuan M, Liu C, Liu W-S, Guo M-N, Morel JL, Huot H, Yu H-J, Tang Y-T, Qiu R-L (2018). Accumulation and fractionation of rare earth elements (REEs) in the naturally grown Phytolacca americana L. in southern China. International Journal of Phytoremediation 20, 415–423.
Accumulation and fractionation of rare earth elements (REEs) in the naturally grown Phytolacca americana L. in southern ChinaCrossref | GoogleScholarGoogle Scholar | 29608375PubMed |

Zhang ZY, Wang YQ, Li FL, Xiao HQ, Chai ZF (2002). Distribution characteristics of rare earth elements in plants from a rare earth ore area. Journal of Radioanalytical and Nuclear Chemistry 252, 461–465.
Distribution characteristics of rare earth elements in plants from a rare earth ore areaCrossref | GoogleScholarGoogle Scholar |

Zhang Z, Sugawara K, Hatayama M, Huang Y, Inoue C (2014). Screening of As-accumulating plants using a foliar application and a native accumulation of As. International Journal of Phytoremediation 16, 257–266.
Screening of As-accumulating plants using a foliar application and a native accumulation of AsCrossref | GoogleScholarGoogle Scholar | 24912222PubMed |

Zhuang M, Wang L, Wu G, Wang K, Jiang X, Liu T, Xiao P, Yu L, Jiang Y, Song J, Zhang J, Zhou J, Zhao J, Chu Z (2017). Health risk assessment of rare earth elements in cereals from mining area in Shandong, China. Scientific Reports 7, 9772
Health risk assessment of rare earth elements in cereals from mining area in Shandong, ChinaCrossref | GoogleScholarGoogle Scholar | 28852170PubMed |