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The translocation and fractionation of rare earth elements (REEs) via the phloem in Phytolacca americana L.

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Abstract

Rare earth elements (REEs) are considered to be emerging contaminants due to their widespread use and lack of recycling. Phytolacca americana L. has great potential for REEs phytoextraction. Our understanding of REEs in P. americana focuses mostly on root absorption and xylem translocation, but the role of phloem translocation has received little attention. In this research, the translocation and fractionation of REEs from phloem to organs in P. americana were investigated. In addition, the effect of organic acids in the REEs translocation via phloem exudates was also examined. The results showed that REEs could transport bidirectionally via the phloem, and 86% of REEs exported from old leaves could move downwards to the root, whereas only 14% of them transported upwards to the young leaves. Heavy rare earth elements (HREEs) enrichment was found in the REEs fractionation processes both from phloem to leaf and from stem to root, indicating that HREEs were preferentially transferred not only down to roots, but also up to the young leaves. The concentration of oxalic acid in phloem exudates was much higher than other organic acids. 94.7% oxalic acid in phloem exudates was preferred to combine with REEs, especially HREEs. Additionally, the concentrations of HREEs had a high positive correlation with oxalic acid in phloem exudates, which demonstrated oxalic acid may play a significant role in the long-distance transport of HREEs in phloem. In conclusion, HREEs have higher translocation ability than light rare earth elements (LREEs) in both xylem and phloem of P. americana. As far as we know, this is the first report focused on the phloem translocation and redistribution of REEs in P. americana, which provides a valuable understanding of the mechanism for phytoremediation of REEs contaminated soils.

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References

  • Ando Y, Nagata S, Yanagisawa S, Yoneyama T (2012) Copper in xylem and phloem saps from rice (Oryza sativa): the effect of moderate copper concentrations in the growth medium on the accumulation of five essential metals and a speciation analysis of copper-containing compounds. Funct Plant Biol 40:89–100

    Google Scholar 

  • Babula P, Adam V, Opatrilova R, Zehnalek J, Havel L, Kizek R (2008) Uncommon heavy metals, metalloids and their plant toxicity: a review. Environ Chem Lett 6:189–213

    CAS  Google Scholar 

  • Balaram V (2019) Rare earth elements: a review of applications, occurrence, exploration, analysis, recycling, and environmental impact. Geosci Front 10:1285–1303

    CAS  Google Scholar 

  • Byrne RH, Li BQ (1995) Comparative complexation behavior of the rare-earths. Geochim Cosmochim Acta 59:4575–4589

    CAS  Google Scholar 

  • Cakmak I, Hengeler C, Marschner H (1994) Changes in phloem export of sucrose in leaves in response to phosphorus, potassium and magnesium-deficiency in bean-plants. J Exp Bot 45:1251–1257

    CAS  Google Scholar 

  • Cao XD, Zhao GW, Yin M, Li JX (1998) Determination of ultratrace rare earth elements in tea by inductively coupled plasma mass spectrometry with microwave digestion and AG50W-x8 cation exchange chromatography. Analyst 123:1115–1119

    CAS  Google Scholar 

  • Cao YN, Ma CX, Chen HJ, Zhang JF, White JC, Chen GC, Xing BS (2020) Xylem-based long-distance transport and phloem remobilization of copper in Salix integra Thunb. J Hazard Mater 392:122428

    CAS  Google Scholar 

  • Centofanti T, Sayers Z, Cabello-Conejo MI, Kidd P, Nishizawa NK, Kakei Y, Davis AP, Sicher RC, Chaney RL (2013) Xylem exudate composition and root-to-shoot nickel translocation in Alyssum species. Plant Soil 373:59–75

    CAS  Google Scholar 

  • Chamel A, Pineri M, Escoubes M (1991) Quantitative-determination of water sorption by plant cuticles. Plant Cell Environ 14:87–95

    Google Scholar 

  • Chao YQ, Liu WS, Chen YM, Chen WH, Zhao LH, Ding QB, Wang SZ, Tang YT, Zhang T, Qiu RL (2016) Structure, variation, and Co-occurrence of soil microbial communities in abandoned sites of a rare earth elements mine. Environ Sci Technol 50:11481–11490

    CAS  Google Scholar 

  • Che Y, Xing R, Zhu YF, Cui YH, Jiang XH (2011) Effects of lanthanum chloride administration on detouring learning in chicks. Biol Trace Elem Res 143:274–280

    CAS  Google Scholar 

  • Deng THB, Tang YT, van der Ent A, Sterckeman T, Echevarria G, Morel JL, Qiu RL (2016) Nickel translocation via the phloem in the hyperaccumulator Noccaea caerulescens (Brassicaceae). Plant Soil 404:35–45

    CAS  Google Scholar 

  • Enot MM, Weiland F, Mittal P, Hoffmann P, Sillero-Mahinay M, Pukala T (2021) Differential proteome analysis of the leaves of lead hyperaccumulator, Rhoeo discolor (L. Her.) Hance. J Mass Spectrom 56:e4689

    CAS  Google Scholar 

  • Erenoglu B, Nikolic M, Romheld V, Cakmak I (2002) Uptake and transport of foliar applied zinc (65Zn) in bread and durum wheat cultivars differing in zinc efficiency. Plant Soil 241:251–257

    CAS  Google Scholar 

  • Fondy BR, Geiger DR (1980) Effect of rapid changes in sink-source ratio on export and distribution of products of photosynthesis in leaves of Beta vulgaris L. and Phaseolus vulgaris L. Plant Physiol 66:945–949

    CAS  Google Scholar 

  • Fredeen AL, Rao IM, Terry N (1989) Influence of phosphorus-nutrition on growth and carbon partitioning in glycine-max. Plant Physiol 89:225–230

    CAS  Google Scholar 

  • Fu HJ, Yu HY, Li TX, Wu Y (2019) Effect of cadmium stress on inorganic and organic components in xylem sap of high cadmium accumulating rice line (Oryza sativa L.). Ecotoxicol Environ Saf 168:330–337

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Guo XS, Zhou Q, Zhu XD, Lu TH, Huang XH (2007) Migration of a rare earth element cerium(III) in horseradish. Acta Chim Sin 65:1922–1924

    CAS  Google Scholar 

  • Guo YY, Chen KY, Lei SH, Gao Y, Yan SP, Yuan M (2023) Rare Earth Elements (REEs) Adsorption and Detoxification Mechanisms in Cell Wall Polysaccharides of Phytolacca americana L. Plants-Basel 12:1981

    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

    CAS  Google Scholar 

  • Harris WR, Sammons RD, Grabiak RC (2012) A speciation model of essential trace metal ions in phloem. J Inorg Biochem 116:140–150

    CAS  Google Scholar 

  • Harvey MA, Erskine PD, Harris HH, Brown GK, Pilon-Smits EAH, Casey LW et al (2020) Distribution and chemical form of selenium in Neptunia amplexicaulisfrom Central Queensland, Australia. Metallomics 12:514–527

    CAS  Google Scholar 

  • Haslett BS, Reid RJ, Rengel Z (2001) Zinc mobility in wheat: uptake and distribution of zinc applied to leaves or roots. Ann Bot 87:379–386

    CAS  Google Scholar 

  • Haydon MJ, Cobbett CS (2007) Transporters of ligands for essential metal ions in plants. New Phytol 174:499–506

    CAS  Google Scholar 

  • Hermans C, Hammond JP, White PJ, Verbruggen N (2006) How do plants respond to nutrient shortage by biomass allocation? Trends Plant Sci 11:610–617

    CAS  Google Scholar 

  • Hu Y, Tian SK, Foyer CH, Hou DD, Wang HX, Zhou WW, Liu T, Ge J, Lu LL, Lin XY (2019) Efficient phloem transport significantly remobilizes cadmium from old to young organs in a hyperaccumulator Sedum alfredii. J Hazard Mater 365:421–429

    CAS  Google Scholar 

  • Kato M, Ishikawa S, Inagaki K, Chiba K, Hayashi H, Yanagisawa S, Yoneyama T (2010) Possible chemical forms of cadmium and varietal differences in cadmium concentrations in the phloem sap of rice plants (Oryza sativa L.). Soil Sci Plant Nutr 56:839–847

    CAS  Google Scholar 

  • Kim MJ, Kim T (2011) Extraction of arsenic and heavy metals from contaminated mine tailings by soil washing. Soil Sediment Contam 20:631–648

    CAS  Google Scholar 

  • Li XF, Chen ZB, Chen ZQ, Zhang YH (2013) A human health risk assessment of rare earth elements in soil and vegetables from a mining area in Fujian Province, Southeast China. Chemosphere 93:1240–1246

    CAS  Google Scholar 

  • Li LP, Zhang YQ, Ippolito JA, Xing WQ, Qiu KY, Wang YL (2020) Cadmium foliar application affects wheat Cd, Cu, Pb and Zn accumulation. Environ Pollut 262:114329

    CAS  Google Scholar 

  • Liu D, Wang X, Lin Y, Chen Z, Xu H, Wang L (2012) The effects of cerium on the growth and some antioxidant metabolisms in rice seedlings. Environ Sci Pollut Res 19:3282–3291

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Liu C, Liu WS, van der Ent A, Morel JL, Zheng HX, Wang GB, Tang YT, Qiu RL (2021) Simultaneous hyperaccumulation of rare earth elements, manganese and aluminum in Phytolacca americana in response to soil properties. Chemosphere 282:131096

    CAS  Google Scholar 

  • Liu C, Sun D, Zheng HX, Wang GB, Liu WS, Cao Y, Tang YT, Qiu RL (2022) The limited exclusion and efficient translocation mediated by organic acids contribute to rare earth element hyperaccumulation in Phytolacca americana. Sci Total Environ 805:150335

    CAS  Google Scholar 

  • Lu L, Tian S, Zhang J, Yang X, Labavitch JM, Webb SM, Latimer M, Brown PH (2013) Efficient xylem transport and phloem remobilization of Zn in the hyperaccumulator plant species Sedum alfredii. New Phytol 198:721–731

    CAS  Google Scholar 

  • Luo Z-B, He J, Polle A, Rennenberg H (2016) Heavy metal accumulation and signal transduction in herbaceous and woody plants: paving the way for enhancing phytoremediation efficiency. Biotechnol Adv 34:1131–1148

    CAS  Google Scholar 

  • Mendoza-Cozatl DG, Butko E, Springer F, Torpey JW, Komives EA, Kehr J, Schroeder JI (2008) Identification of high levels of phytochelatins, glutathione and cadmium in the phloem sap of Brassica napus. A role for thiol-peptides in the long-distance transport of cadmium and the effect of cadmium on iron translocation. Plant J 54:249–259

    CAS  Google Scholar 

  • Millero FJ (1992) Stability constants for the formation of rare-earth inorganic complexes as a function of ionic strength. Geochim Cosmochim Acta 56:3123–3132

    CAS  Google Scholar 

  • Milner MJ, Kochian LV (2008) Investigating heavy-metal hyperaccumulation using Thlaspi caerulescens as a model system. Ann Bot 102:3–13

    CAS  Google Scholar 

  • Mohamed Ahmed Al-Qahtani K (2017) Extraction heavy metals from contaminated water using chelating agents. Orient J Chem 33:1698–1704

    Google Scholar 

  • Ozaki T, Suzuki Y, Nankawa T, Yoshida T, Ohnuki T, Kimura T, Francis AJ (2006) Interactions of rare earth elements with bacteria and organic ligands. J Alloys Compd 408:1334–1338

    Google Scholar 

  • Pablo Lozano R, Perez-de la Fuente R, Barron E, Rodrigo A, Luis Viejo J, Penalver E (2020) Phloem sap in Cretaceous ambers as abundant double emulsions preserving organic and inorganic residues. Sci Rep 10:9751

    Google Scholar 

  • Page V, Weisskopf L, Feller U (2006) Heavy metals in white lupin: uptake, root-to-shoot transfer and redistribution within the plant. New Phytol 171:329–341

    CAS  Google Scholar 

  • Persanov VM, Andreeva TF (1970) Effect of duration of phosphorus deficiency on transfer and utilization of assimilates with regard to plant growth and productivity. Fiziol Rast 17:1175–1181

    Google Scholar 

  • Pourrut B, Shahid M, Dumat C, Winterton P, Pinelli E (2011) Lead uptake, toxicity, and detoxification in plants. Rev Environ Contam Toxicol 213:113–136

    CAS  Google Scholar 

  • Radin JW, Eidenbock MP (1984) Hydraulic conductance as a factor limiting leaf expansion of phosphorus-deficient cotton plants. Plant Physiol 75:372–377

    CAS  Google Scholar 

  • Rao IM, Fredeen AL, Terry N (1990) Leaf phosphate status, photosynthesis, and carbon partitioning in sugar beet: III. Diurnal changes in carbon partitioning and carbon export. Plant Physiol 92:29–36

    CAS  Google Scholar 

  • Sadeghi M, Petrosino P, Ladenberger A, Albanese S, Andersson M, Morris G, Lima A, De Vivo B, Team GP (2013) Ce, La and Y concentrations in agricultural and grazing-land soils of Europe. J Geochem Explor 133:202–213

    CAS  Google Scholar 

  • Saifullah SM, Zia-Ur-Rehman M, Sabir M, Ahmad HR (2015) Chapter 14 - Phytoremediation of Pb-contaminated soils using synthetic chelates. In: Hakeem KR (ed) Soil Remediation and Plants. Academic Press, San Diego, pp 397–414

    Google Scholar 

  • Shan XQ, Wang HI, Zhang SZ, Zhou HF, 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

    CAS  Google Scholar 

  • Shen RF, Ma JF (2001) Distribution and mobility of aluminium in an Al-accumulating plant, Fagopyrum esculentum Moench. J Exp Bot 52:1683–1687

    CAS  Google Scholar 

  • Tetyuk O, Benning UF, Hoffmann-Benning S (2013) Collection and analysis of Arabidopsis phloem exudates using the EDTA-facilitated method. J vis Exp 26:e51111

    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 RL, Mulligan DR (2015) Agromining: farming for metals in the future? Environ Sci Technol 49:4773–4780

    Google Scholar 

  • Vitkova M, Komarek M, Tejnecky V, Sillerova H (2015) Interactions of nano-oxides with low-molecular-weight organic acids in a contaminated soil. J Hazard Mater 293:7–14

    CAS  Google Scholar 

  • Wang LH, Li JG, Zhou Q, Yang GM, Ding XL, Li XD, Cai CX, Zhang Z, Wei HY, Lu TH, Deng XW, Huang XH (2014) Rare earth elements activate endocytosis in plant cells. Proc Natl Acad Sci U S A 111:12936–12941

    CAS  Google Scholar 

  • Wei Z, Hong F, Yin M, Li H, Hu F, Zhao G, Wong JW (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

    CAS  Google Scholar 

  • Wu JL, Chen AQ, Peng SL, Wei ZG, Liu GC (2013) Identification and application of amino acids as chelators in phytoremediation of rare earth elements lanthanum and yttrium. Plant Soil 373:329–338

    CAS  Google Scholar 

  • Yang M, Wu JC, Gu HN (2012) Study of the relationship between the content of the rare earth element Eu in rice plants and in Nilaparvata lugens (Hemiptera: Delphacidae). Insect Science 19:13–20

    CAS  Google Scholar 

  • Yoneyama T, Gosho T, Kato M, Goto S, Hayashi H (2010) Xylem and phloem transport of Cd, Zn and Fe into the grains of rice plants (Oryza sativa L.) grown in continuously flooded Cd-contaminated soil. Soil Sci Plant Nutr 56:445–453

    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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Zeng Q, Zhu JG, Cheng HL, Xie ZB, Chu HY (2006) Phytotoxicity of lanthanum in rice in haplic acrisols and cambisols. Ecotoxicol Environ Saf 64:226–233

    CAS  Google Scholar 

  • Zeng QL, Chen RF, Zhao XQ, Shen RF, Noguchi A, Shinmachi F, Hasegawa I (2013) Aluminum could be transported via phloem in Camellia oleifera Abel. Tree Physiol 33:96–105

    CAS  Google Scholar 

  • Zhao YP, Cui JL, Chan TS, Dong JC, Chen DL, Li XD (2018) Role of chelant on Cu distribution and speciation in Lolium multiflorum by synchrotron techniques. Sci Total Environ 621:772–781

    CAS  Google Scholar 

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Funding

We thank the Wuhan Institute of Technology for supporting this research. This research was supported by National Natural Science Foundation of China (41907136), and Graduate Innovative Fund of Wuhan Institute of Technology (CX2021450).

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Authors and Affiliations

  1. Key Laboratory of Green Chemical Engineering Process of Ministry of Education, School of Environmental Ecology and Biological Engineering, Wuhan Institute of Technology, Wuhan, 430205, China

    Yingying Guo, Shengwen Xu, Shengpeng Yan, Shihan Lei, Yuan Gao, Keyi Chen, Xiaoyu Shi, Ming Yuan & Huaiying Yao

  2. Key Laboratory of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen, 361021, China

    Huaiying Yao

  3. Zhejiang Key Laboratory of Urban Environmental Processes and Pollution Control, Ningbo Urban Environment Observation and Research Station, Chinese Academy of Sciences, Ningbo, China

    Huaiying Yao

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  1. Yingying Guo
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  2. Shengwen Xu
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  4. Shihan Lei
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Contributions

All authors contributed to the study conception & design, and agree to publish the work in this journal. Material preparation was performed by Shihan Lei, Yuan Gao, Keyi Chen and Xiaoyu Shi. Data collection and analysis were performed by Yingying Guo, Shengwen Xu and Shengpeng Yan. The first draft of the manuscript was written by Yingying Guo and all authors commented on previous versions of the manuscript. Writing review and editing was performed by Ming Yuan and Huaiying Yao. All authors read and approved the final manuscript.

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Correspondence to Ming Yuan.

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Highlights

• First report of rare earth elements translocation via phloem in hyperaccumulator

• REEs were transported bidirectionally via the phloem in Phytolacca americana

• HREEs were preferentially transferred to both roots and young leaves via phloem

• Oxalic acid is important to the long-distance translocation of HREEs via phloem

• Conceptual model for REEs translocation via xylem and phloem is constructed

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Guo, Y., Xu, S., Yan, S. et al. The translocation and fractionation of rare earth elements (REEs) via the phloem in Phytolacca americana L.. Environ Sci Pollut Res 30, 114044–114055 (2023). https://doi.org/10.1007/s11356-023-30473-0

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