Abstract
Plants that naturally accumulate aluminium (Al) may also inadvertently accumulate rare earth elements (REEs) due to the similar chemical properties of Al and REE trivalent ions, and vice versa. In this study, an Al hyperaccumulator plant species, Melastoma malabathricum, and a species known to have a propensity to hyperaccumulate REEs (in addition to Al), Dicranopteris linearis, were evaluated for potential REE accumulation in a one-year pot dosing trial in Sabah, Malaysia. To test whether the Malaysian accessions of D. linearis and M. malabathricum hyperaccumulate REEs (and Al), both species were grown in pots containing soil treated with solutions containing yttrium (Y), lanthanum (La), neodymium (Nd), and a mixture of these three REEs. The results showed that both M. malabathricum and D. linearis accumulated > 1000 µg g−1 Al in their leaves as expected. The shoots of M. malabathricum contained lower REEs than the roots (50 µg g−1 compared to 905 µg g−1). In D. linearis, the mean foliar REE concentrations ranged from 145 to 315 µg g−1, which is below the hyperaccumulation threshold set for REEs (> 1000 µg g−1 REEs). This study revealed that the Malaysian accessions of both M. malabathricum and D. linearis are Al hyperaccumulators, but their REE hyperaccumulation status requires further testing.
This is a preview of subscription content, log in via an institution to check access.
References
Brown PH, Rathjen AH, Graham RD, Tribe DE (1990) Rare earth elements in biological systems. Handb Phys Chem Rare Earth 13:423–452
Cao X, Chen Y, Gu Z, Wang X (2000) Determination of trace rare earth elements in plant and soil samples by Inductively Coupled Plasma-Mass Spectrometry. Int J Environ Anal Chem 76:295–309. https://doi.org/10.1080/03067310008034137
Carr HP, Lombi E, Küpper H et al (2003) Accumulation and distribution of aluminium and other elements in tea (Camellia sinensis) leaves. Agronomie 23:705–710. https://doi.org/10.1051/agro:2003045
Chour Z, Laubie B, Morel JL et al (2018) Recovery of rare earth elements from Dicranopteris dichotoma by an enhanced ion exchange leaching process. Chem Eng Process Process Intensif 130:208–213. https://doi.org/10.1016/j.cep.2018.06.007
Chour Z, Laubie B, Morel JL et al (2020) Basis for a new process for producing REE oxides from Dicranopteris linearis. J Environ Chem Eng 8:103961. https://doi.org/10.1016/j.jece.2020.103961
Clarkson DT (1965) The effect of aluminium and some other trivalent metal cations on cell division in the root apices of Allium cepa. Ann Bot 29:309–315. https://doi.org/10.1093/oxfordjournals.aob.a083953
Delhaize E, Ryan PR (1995) Aluminum toxicity and tolerance in plants. Plant Physiol 107:315–321. https://doi.org/10.1104/pp.107.2.315
Funk JL, Amatangelo KL (2013) Physiological mechanisms drive differing foliar calcium content in ferns and angiosperms. Oecologia 173:23–32. https://doi.org/10.1007/s00442-013-2591-1
Haruyama Y, Fujiwara T, Yasuda K et al (2019) Localization of aluminum in epidermal cells of mature tea leaves. Quantum Beam Sci 3:9. https://doi.org/10.3390/qubs3020009
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
Jansen S, Broadley MR, Robbrecht E, Smets E (2002) Aluminum hyperaccumulation in angiosperms: a review of its phylogenetic significance. Bot Rev 68:235–269
Joffry SM, Yob NJ, Rofiee MS et al (2012) Melastoma malabathricum (L.) smith ethnomedicinal uses, chemical constituents, and pharmacological properties: a review. Evid Based Compl Altern Med 2012:1–48. https://doi.org/10.1155/2012/258434
Kabata-Pendias A (2010) Trace elements in soils and plants, 4th edn. CRC Press, New York
Khairil M, Burslem DFRP (2018) Controls on foliar aluminium accumulation among populations of the tropical shrub Melastoma malabathricum L. (Melastomataceae). Tree Physiol 38:1752–1760. https://doi.org/10.1093/treephys/tpy082
Khan AM, Yusoff I, Abu-Bakar NK et al (2017) Accumulation, uptake and bioavailability of rare earth elements (REEs) in soil grown plants from ex-mining area in Perak, Malaysia. Appl Ecol Environ Res 15:117–133. https://doi.org/10.15666/aeer/1503_117133
Kopittke PM (2016) Role of phytohormones in aluminium rhizotoxicity. Plant Cell Environ 39:2319–2328. https://doi.org/10.1111/pce.12786
Kopittke PM, McKenna BA, Blamey FPC et al (2009) Metal-induced cell rupture in elongating roots is associated with metal ion binding strengths. Plant Soil 322:303–315. https://doi.org/10.1007/s11104-009-9917-0
Kopittke PM, Menzies NW, Wang P, Blamey FPC (2016) Kinetics and nature of aluminium rhizotoxic effects: a review. J Exp Bot 67:4451–4467. https://doi.org/10.1093/jxb/erw233
Koyama M, Shirakawa M, Takada J et al (1987) Trace elements in land plants: Concentration ranges and accumulators of rare earths, Ba, Ra, Mn, Fe, Co and heavy halogens. J Radioanal Nucl Chem Artic 112:489–506. https://doi.org/10.1007/BF02132381
Liu D, Wang X, Chen X et al (2012) Effects of lanthanum on the change of calcium level in the root cells of rice. Commun Soil Sci Plant Anal 43:1994–2003. https://doi.org/10.1080/00103624.2012.693231
Liu W-S, van der Ent A, Erskine PD, Morel JL, Echevarria G, Spiers KM, Montargès-Pelletier E, Qiu R-L, Tang Y-T (2020) Spatially resolved localization of lanthanum and cerium in the rare earth element hyperaccumulator fern Dicranopteris linearis from China. Environ Sci Technol 54:2287–2294
Liu WS, Zheng HX, Guo MN et al (2019) Co-deposition of silicon with rare earth elements (REEs) and aluminium in the fern Dicranopteris linearis from China. Plant Soil 437:427–437. https://doi.org/10.1007/s11104-019-04005-0
Ma JF, Hiradate S (2000) Form of aluminium for uptake and translocation in buckwheat (Fagopyrum esculentum Moench). Planta 211:355–360. https://doi.org/10.1007/s004250000292
Ma JF, Ryan PR, Delhaize E (2001) Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci 6:273–278. https://doi.org/10.1016/S1360-1385(01)01961-6
Nkrumah PN, Echevarria G, Erskine PD et al (2019) Growth effects in tropical nickel-agromining ‘metal crops’’ in response to nutrient dosing’. J Plant Nutr Soil Sci 182:715–728. https://doi.org/10.1002/jpln.201800468
Pletnev IV, Zernov VV (2002) Classification of metal ions according to their complexing properties: a data-driven approach. Anal Chim Acta 455:131–142. https://doi.org/10.1016/S0003-2670(01)01571-9
Pollard AJ, Powell KD, Harper FA, Smith JAC (2002) The genetic basis of metal hyperaccumulation in plants. CRC Crit Rev Plant Sci 21:539–566. https://doi.org/10.1080/0735-260291044359
Poschenrieder C, Barceló J (2013) Aluminum in plants. Encyclopedia of Metalloproteins. Springer, New York, pp 34–38
Redling K (2006) Rare earth elements in agriculture with emphasis on animal husbandry. LMU, München
Reid RJ, Rengel Z, Smith FA (1996) Membrane fluxes and comparative toxicities of aluminium, scandium and gallium. J Exp Bot 47:1881–1888. https://doi.org/10.1093/jxb/47.12.1881
Robinson WO (1943) The occurrence of rare earths in plants and soils. Soil Sci 56:1–6. https://doi.org/10.1097/00010694-194307000-00001
Roy AK, Sharma A, Talukder G (1988) Some aspects of aluminum toxicity in plants. Bot Rev 54:145–178. https://doi.org/10.1007/BF02858527
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. https://doi.org/10.1046/j.1365-2745.1998.8650765.x
Saat A, Kamsani AS, Kamri WNAN, et al (2015) Potential of Melastoma malabathricum as bio-accumulator for uranium and thorium from soil. In: AIP Conference Proceedings. p 050001
Selamat SN, Abdullah SRS, Idris M (2014) Phytoremediation of lead (Pb) and arsenic (As) by Melastoma malabathricum L. from contaminated soil in separate exposure. Int J Phytoremediation 16:694–703. https://doi.org/10.1080/15226514.2013.856843
Shan X, Wang H, Zhang S et al (2003) Accumulation and uptake of light rare earth elements in a hyperaccumulator Dicropteris dichotoma. Plant Sci 165:1343–1353. https://doi.org/10.1016/S0168-9452(03)00361-3
Thomas PJ, Carpenter D, Boutin C, Allison JE (2014) Rare earth elements (REEs): Effects on germination and growth of selected crop and native plant species. Chemosphere 96:57–66. https://doi.org/10.1016/j.chemosphere.2013.07.020
Van der Ent A, Przybyłowicz WJ, de Jonge MD, Harris HH, Ryan CG, Tylko G, Paterson DJ, Barnabas AD, Kopittke PM, Mesjasz-Przybyłowicz J (2018) X-ray elemental mapping techniques for elucidating the ecophysiology of hyperaccumulator plants. New Phytol 218:432–452
Waller RA, Duncan DB (1969) A bayes rule for the symmetric multiple comparisons problems. J Am Stat Assoc 64:1484. https://doi.org/10.2307/2286085
Wang WCT, Wang H (1998) Research advance on interaction between metal ion of REEs and enzyme molecule. Chinese Rare Earths (in Chinese) 19:57–65
Wang H, Shan X, Zhang S, Wen B (2003) Preliminary characterization of a light-rare-earth-element-binding peptide of a natural perennial fern Dicranopteris dichotoma. Anal Bioanal Chem 376:49–52. https://doi.org/10.1007/s00216-003-1853-x
Wang LF, Ji HB, Bai KZ et al (2005) Photosynthetic characterization of the plant Dicranopteris dichotoma Bernh. in a rare earth elements mine. J Integr Plant Biol 47:1092–1100. https://doi.org/10.1111/j.1744-7909.2005.00138.x
Wang L, Li J, Zhou Q et al (2014) Rare earth elements activate endocytosis in plant cells. Proc Natl Acad Sci USA 111:12936–12941. https://doi.org/10.1073/pnas.1413376111
Watanabe T, Osaki M (2002) Role of organic acids in aluminum accumulation and plant growth in Melastoma malabathricum. Tree Physiol 22:785–792. https://doi.org/10.1093/treephys/22.11.785
Watanabe T, Osaki M (2009) Possible reasons why aluminum is a beneficial element for Melastoma malabathricum, an aluminum accumulator. In: The Proceedings of the International Plant Nutrition Colloquium XVI
Watanabe T, Osaki M, Tadano T (1997) Aluminum-induced growth stimulation in relation to calcium, magnesium, and silicate nutrition in Melastoma malabathricum l. Soil Sci Plant Nutr 43:827–837. https://doi.org/10.1080/00380768.1997.10414649
Watanabe T, Osaki M, Yoshihara T, Tadano T (1998) Distribution and chemical speciation of aluminum in the Al accumulator plant, Melastoma malabathricum L. Plant Soil 201:165–173. https://doi.org/10.1023/A:1004341415878
Watanabe T, Jansen S, Osaki M (2005a) The beneficial effect of aluminium and the role of citrate in Al accumulation in Melastoma malabathricum. New Phytol 165:773–780. https://doi.org/10.1111/j.1469-8137.2004.01261.x
Watanabe T, Misawa S, Osaki M (2005b) Aluminum accumulation in the roots of Melastoma malabathricum, an aluminum-accumulating plant. Can J Bot 83:1518–1522. https://doi.org/10.1139/b05-111
Watanabe T, Misawa S, Hiradate S, Osaki M (2008) Root mucilage enhances aluminum accumulation in Melastoma malabathricum, an aluminum accumulator. Plant Signal Behav 3:603–605. https://doi.org/10.4161/psb.3.8.6356
Wei Z, Hong F, Yin M et al (2005) Structural differences between light and heavy rare earth element binding chlorophylls in naturally grown fern Dicranopteris linearis. Biol Trace Elem Res 106:279–297. https://doi.org/10.1385/BTER:106:3:279
White PJ, Broadley MR (2003) Calcium in plants. Ann Bot 92:487–511. https://doi.org/10.1093/aob/mcg164
Yuan M, Guo MN, Liu WS et al (2017) The accumulation and fractionation of Rare Earth Elements in hydroponically grown Phytolacca americana L. Plant Soil 421:67–82. https://doi.org/10.1007/s11104-017-3426-3
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. Int J Phytoremediation 20:415–423
Zhenggui W (2006) Research trends on rare earth element hyperaccumulator. J Chinese Rare Earth Soc 1:1–11
Zhenggui W, Ming Y, Xun Z et al (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. https://doi.org/10.1016/S0269-7491(00)00240-2
Acknowledgements
Imam Purwadi and Adrian Paul were the recipients of Australian Government Research Training Program Scholarships and UQ Centennial Scholarships at The University of Queensland, Australia. We acknowledge Sabah Parks for permission to conduct this research at Monggis substation. We thank Sukaibin Sumail for his support during the project and Deisie Suin, Richard Yulong, Weiter Minas and Vinson Yempios for their help in the nursery.
Funding
No funding was received for conducting this study.
Author information
Authors and Affiliations
Contributions
ALDP, PNN and AVDE designed and conducted the experiment. PNN and AVDE collected the samples and undertook the chemical analysis of the samples. IM and PNN performed data processing and analysis. All authors contributed to writing of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflicts of interest to declare that are relevant to the content of this article.
Additional information
Communicated by Marko Rohlfs.
Rights and permissions
About this article
Cite this article
Purwadi, I., Nkrumah, P.N., Paul, A.L.D. et al. Uptake of yttrium, lanthanum and neodymium in Melastoma malabathricum and Dicranopteris linearis from Malaysia. Chemoecology 31, 335–342 (2021). https://doi.org/10.1007/s00049-021-00348-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00049-021-00348-2