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Uptake of rare earth elements by citrus plants from phosphate fertilizers

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Christian Turra
Christian Turra
Christian Turra
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Elisabete A. De Nadai Fernandes at University of São Paulo
Elisabete A. De Nadai Fernandes
Marcio Arruda Bacchi at University of São Paulo
Marcio Arruda Bacchi
Gabriel Adrián Sarriés
Gabriel Adrián Sarriés
Gabriel Adrián Sarriés
  • This person is not on ResearchGate, or hasn't claimed this research yet.
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Abstract and Figures

Background and Aims Rare earth elements (REE) are a group of the periodic table formed by 17 chemical elements (lanthanoids plus yttrium and scandium). They have been used in different field applications. In agriculture, they can be found in some phosphate fertilizers at levels one or two orders of magnitude higher than those found in normal agricultural soils. Citrus plants are known to present high levels of REE when compared to most other species, however, there is little information about bioavailability of REE in phosphate fertilizers for citrus plants. This work focuses on the study of REE behavior by the application of increasing doses of single superphosphate fertilizer in Rangpur lime (Citrus limonia Osbeck) plants in a greenhouse study. Methods The technique used was instrumental neutron activation analysis (INAA). Results The results showed that the fertilizer has caused significant increases in the content of REE in the citrus plant tissues, with higher concentrations in leaves than in branches. The highest substrate-leaf transfer factor was observed for La (0.0047), though the concentrations in the plants followed the same order found in the substrate, i.e. Ce > La > Sm > Eu > Sc. Conclusion There was an increase of rare earth elements concentrations in Rangpur lime plants by superphosphate fertilizer application.
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REGULAR ARTICLE
Uptake of rare earth elements by citrus plants from phosphate
fertilizers
Christian Turra &Elisabete A. De Nadai Fernandes &
Márcio Arruda Bacchi &Gabriel Adrián Sarriés &
Andrés Enrique Lai Reyes
Received: 31 October 2018 /Accepted: 30 January 2019 / Published online: 13 February 2019
#Springer Nature Switzerland AG 2019
Abstract
Background and Aims Rare earth elements (REE) are a
group of the periodic table formed by 17 chemical
elements (lanthanoids plus yttrium and scandium). They
have been used in different field applications. In agri-
culture, they can be found in some phosphate fertilizers
at levels one or two orders of magnitude higher than
those found in normal agricultural soils. Citrus plants
are known to present high levels of REE when com-
pared to most other species, however, there is little
information about bioavailability of REE in phosphate
fertilizers for citrus plants. This work focuses on the
study of REE behavior by the application of increasing
doses of single superphosphate fertilizer in Rangpur
lime (Citrus limonia Osbeck) plants in a greenhouse
study.
Methods The technique used was instrumental neutron
activation analysis (INAA).
Results The results showed that the fertilizer has caused
significant increases in the content of REE in the citrus
plant tissues, with higher concentrations in leaves than
in branches. The highest substrate-leaf transfer factor
was observed for La (0.0047), though the concentrations
in the plants followed the same order found in the
substrate, i.e. Ce > La > Sm > Eu > Sc.
Conclusion There was an increase of rare earth ele-
ments concentrations in Rangpur lime plants by super-
phosphate fertilizer application.
Keywords Rare earth elements .Citrus plants .
Lanthanoids .Phosphate fertilizers .Bioavailability
Introduction
The group of rare earth elements (REE) is composed by
lanthanoids (La, Ce, Pr, Nd, Pm, Sm, Eu, Gd, Tb, Dy,
Ho, Er, Tm, Yb and Lu) plus Y and Sc. They have
similar physical and chemical properties (Henderson
1984) and are trivalent, with exception of some elements
that present two different oxidation states, i.e. Ce (3+
and 4+), Sm (2+ and 3+), Eu (2+ and 3+), Nd (3+ and
Plant Soil (2019) 437:291–299
https://doi.org/10.1007/s11104-019-03979-1
Responsible Editor: Juan Barcelo.
C. Turra :E. A. De Nadai Fernandes :M. A. Bacchi (*)
Centro de Energia Nuclear na Agricultura, Universidade de São
Paulo (CENA/USP), Avenida Centenário, 303, Piracicaba, SP
13416-000, Brazil
e-mail: mabacchi@cena.usp.br
C. Turra
e-mail: agrochri2010@gmail.com
E. A. De Nadai Fernandes
e-mail: lis@cena.usp.br
G. A. Sarriés :A. E. L. Reyes
Escola Superior de Agricultura Luiz de Queiroz, Universidade de
São Paulo (ESALQ/USP), Avenida Pádua Dias, 11, Piracicaba, SP
13418-900, Brazil
G. A. Sarriés
e-mail: gasarrie@usp.br
A. E. L. Reyes
e-mail: lai@usp.br
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... Specifically, some REEs can replace Ca 2+ and Mg 2+ in chloroplasts and chlorophyll, respectively, effectively elevating the activity of Ca-ATPase, ATP synthesis, and photosynthetic rates (Wang et al., 2014;Wei et al., 2005;Yao et al., 2021;Zhou et al., 2011). However, accumulation and adverse effects of REEs were also documented, including growth inhibition, biomass reduction, phytotoxic effects, and inhibition and damage to chloroplasts and photosynthesis (Hu et al., 2016;Pellegrino et al., 2022;Thomas et al., 2014;Turra et al., 2019). Altogether, adjusting the balance between benefits and adverse effects of REEs on plants requires an extensive understanding of the mechanisms by which REEs affect plants. ...
... The accumulation of REEs and other elements (Mg, Al, Ca, Mn, Fe, Co, Cu, V, Ga, Ge, Cd, Sn, Cs, Ba, Pb and Th) in the decreasing order of root>leaves>stems>fruit is a common feature in terrestrial vegetation (Tao et al., 2022), as it has been investigated for both native and crop plants (Brioschi et al., 2013;Carpenter et al., 2015;Turra et al., 2019;Xu et al., 2002). This trend is likely associated with the uptake of elements, including REEs, by root systems followed by transport via the xylem and/or phloem to the leaves, which are considered sinks for most mineral nutrients (Brioschi et al., 2013;Hopkins and Huner, 2009). ...
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... REEs are widely used in industry, agriculture, medicine and other fields owing to their special light, electrical, and magnetic properties (Deng et al. 2022;Xu et al. 2020;Younis et al. 2021). In particular, since the discovery in 1917 that Ce in REEs can promote photosynthesis of plants (Chien 1917), fertilizers containing REEs (e.g., La and Ce) have been applied to crops (Lian et al. 2019;Tommasi et al. 2021;Turra et al. 2019). REE-based fertilizers are mainly applied to crops by aerial or soil-based methods (Cheng et al. 2021a;Lian et al. 2019;Turra et al. 2019). ...
... In particular, since the discovery in 1917 that Ce in REEs can promote photosynthesis of plants (Chien 1917), fertilizers containing REEs (e.g., La and Ce) have been applied to crops (Lian et al. 2019;Tommasi et al. 2021;Turra et al. 2019). REE-based fertilizers are mainly applied to crops by aerial or soil-based methods (Cheng et al. 2021a;Lian et al. 2019;Turra et al. 2019). Over a century of researches have confirmed that the agricultural use of REEs promotes crop photosynthesis, growth and yields (Cheng et al. 2021a;Tao et al. 2022). ...
Endocytosis of root cells induced by low-dose lanthanum(III) can promote seedling photomorphogenesis and leaf photosynthesis
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Background and aims Low-dose lanthanum [La(III)] promotes photosynthesis when applied to plant roots or leaves (i.e., by activating leaf endocytosis), but its mechanism remains unclear. After phenotypic transition from skotomorphogenesis to photomorphogenesis, plants are characterized by inhibition of hypocotyl elongation, chloroplast formation, etc. This study aimed to investigate whether low-dose La(III) could induce root endocytosis to stimulate morphogenesis and promote subsequent photosynthesis of plants. Methods Low-dose (15, 30 μmol L⁻¹) La(III) acted on plant roots, and cell imaging was used to observe endocytosis and Zn(II) in root cells. Technique for metallomics was used to detect nutrient contents in root cells and MS media. Real-time photomicrography was used to measure the bending angle of apical hook during skotomorphogenesis and photomorphogenesis. Twelve photosynthesis-related parameters and two growth parameters were selected to evaluate photosynthesis and growth of plants. Results Low-dose La(III) induced endocytosis in root cells, which transported nutrients to root cells from medium. The sudden increase of nutrient contents in root cells stimulated seedling morphogenesis, i.e., the bending angle of the apical hook in skotomorphogenesis and photomorphogenesis maximally changed by 29.03% and 16.62%, accompanying inhibition of hypocotyl elongation, cotyledon opening and chloroplast formation. The accelerated morphological development further caused the maximum increase in photosynthesis by 66.67%, while total dry weight and leaf area maximally increased by 73.00% and 63.16%, respectively. Conclusion Our study clarified the mechanism by which low-dose La(III) led to a sudden increase in nutrient contents in root cells by inducing endocytosis, thereby promoting seedling photomorphogenesis, plant photosynthesis and growth.
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... However, it is worth noting that heavy metal elements, such as As, Al, Cd, and Pd, are environmental contaminants that can have serious safety risks to plant growth and human health (Czech et al., 2021). Additionally, the uptake properties of rare earth elements, including Ce, La, Sm, Eu, and Sc, in citrus plants were reported (Turra et al., 2019). These results suggested that risk prevention of heavy metals and rare elements in citrus fruits should be performed via monitoring and controlling for a healthy dietary supply. ...
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... However, it is worth noting that heavy metal elements, such as As, Al, Cd, and Pd, are environmental contaminants that can have serious safety risks to plant growth and human health (Czech et al., 2021). Additionally, the uptake properties of rare earth elements, including Ce, La, Sm, Eu, and Sc, in citrus plants were reported (Turra et al., 2019). These results suggested that risk prevention of heavy metals and rare elements in citrus fruits should be performed via monitoring and controlling for a healthy dietary supply. ...
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Article
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Introduction Citrus fruit is considered a superfood due to its multiple nutritional functions and health benefits. Quantitative analysis of the numerous quality characteristics of citrus fruit is required to promote its sustainable production and industrial utilization. However, little information is available on the comprehensive quality assessment of various fruit quality indicators in different citrus cultivars. Methods A total of nine different fresh citrus fruits containing seeds were collected as the experimental materials. The objectives of this study were: (i) to determine the morphological and juice properties of citrus fruits, (ii) to measure the mineral elements in the peel, pulp, and seeds, and (iii) to evaluate the fruit quality index (FQI) using the integrated quality index (IQI) and the Nemoro quality index (NQI) methods. Results There were significant differences in fruit quality characteristics, including morphological, mineral, and juice quality, among the investigated citrus cultivars. The proportion of pulp biomass was the highest, followed by that of peel and seeds. N and Cu had the highest and lowest concentrations, respectively, among the measured elements across all citrus fruits, and the amounts of N, P, Mg, Cu, and Zn in seeds, K and Al in pulp, and Ca, Fe, and Mn in peel were the highest, dramatically affecting the accumulation of minerals in the whole fruit and their distribution in various fruit parts. Additionally, Ningmeng fruits had the highest vitamin C and titratable acidity (TA) but the lowest total soluble solids (TSS) and total phenolic (TP) contents, resulting in the lowest TSS/TA and pH values. In contrast, Jinju fruits had the highest TSS and TP contents. Based on the mineral element and juice quality parameters, principal component analysis showed that the citrus fruits were well separated into four groups, and the dendrogram also showed four clusters with different distances. The FQI range based on the IQI method (FQIIQI) and NQI method (FQINQI) was 0.382-0.590 and 0.106-0.245, respectively, and a positive relationship between FQIIQI and FQINQI was observed. Conclusion Our results highlight the great differences in mineral and juice characteristics among fruit parts, which mediated fruit quality. The strategy of fruit quality assessment using the FQI can be expanded for targeted utilization in the citrus industry.
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... Pachystroma longifolium, Solanum lycocarpum, and Citrus spp. have a high accumulation of REEs in the aboveground part [129][130][131]. The ramie planted in mine sites can be used not only for vegetation restoration and phytostabilization of ion adsorbed rare earth tailings, but also for biomass production with a lower capacity to accumulate REEs [132]. ...
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... In contrast, Turra et al. [73] observed transfer factors of La ranging from 0.62 to 1.09 in citrus plants, which is mentioned among species with a good ability to accumulate REY. In a recent study by the same author, the highest transfer factor of REY was observed for La (0.0047) in Rangpur lime (Citrus limonia Osbeck) plants [74]. These differences can be attributed to soil properties, soil management, planting age and cultivation environments [68,75,76]. ...
Effects of long-term phosphate fertilization on potential risks of emerging contaminants in agroecosystems of the eastern Amazon, Brazil
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This study aimed to assess the levels of rare earth elements and yttrium (REY) and vanadium (V) in soils cultivated with citrus, oil palm and black pepper in the eastern Amazon . The potential risk of contamination was estimated using the enrichment (EF) and bioaccumulation (BAF) factors. The results showed that pH, K, and P significantly affected the REY concentrations. The bioaccumulation of europium was the most significant among the studied elements. The contents of V were positively correlated with pH and Fe and K oxides. The EF and BAF of V followed the order: EF – black pepper (2.95) > oil palm (2.77) ≫ citrus (0.57); BAF – citrus (0.091) > black pepper (0.023) > oil palm (0.018). The increase in REY and V does not pose current risks in the study area. However, these results may support the monitoring of environmental contamination, prevention, and control of emerging contaminants by government agencies.
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Rare earth elements (REEs) are pivotal for advanced technologies, driving a surge in global demand. Import dependency on clean energy minerals raises concerns about supply chain vulnerabilities and geopolitical risks. Conventional REEs productionis resource-intensive and environmentally harmful, necessitating a sustainable supply approach. Phytomining (agromining) utilizes plants for eco-friendly REE extraction, contributing to the circular economy and exploiting untapped metal resources in enriched soils. Critical parameters like soil pH, Casparian strip, and REE valence influence soil and plant uptake bioavailability. Hyperaccumulator species efficiently accumulate REEs, serving as energy resources. Despite a lack of a comprehensive database, phytomining exhibits lower environmental impacts due to minimal chemical usage and CO2 absorption. This review proposes phytomining as a system for REEs extraction, remediating contaminated areas, and rehabilitating abandoned mines. The phytomining of REEs offers a promising avenue for sustainable REEs extraction but requires technological advancements to realize its full potential.
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The rare earth elements (REEs) comprise a group of 16 chemically very similar elements that occur widespread in rocks, soils, and water bodies, share similar ionic radii to the essential element Ca2+, and consequently also occur in biota. Given that REEs form mainly trivalent cations, they also share similarities to Al3+. Compared to their chemical cognate Ca, they have a higher reactivity. Thus, their accumulation in soils may constitute a severe environmental threat. Over the last decades, the increasing use of REEs in modern technology and fertilizers raised concerns about the pollution of soils and water bodies, which led to a rapidly increasing number of publications dealing with REE toxicity to plants, animals and humans, the fate of REE in soil–plant systems, REE cycling in ecosystems and impacts of REE pollution on food security. This review aims to give an overview of the current knowledge on the occurrence of REE in the total environment, including relevant environmental processes governing their mobility, chemical speciation and transfer from abiotic compartments into biota. Beginning with an overview of analytical approaches, we summarize the current knowledge on the ecology of REE in the lithosphere, pedosphere, hydrosphere and biosphere, including impacts of soil pollution on food security and public health.
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The detection of gamma rays induced in soil by naturally occurring cosmic ray neutrons is explored with the Geant4 Simulation Toolkit to monitor carbon sequestration in soil. The simulated soil is a uniform mixture of minerals, air, water, and soil organic carbon. As the soil organic carbon increases from 0% to 15% by volume, the mineral matter decreases, and gamma ray counts from mineral-related isotopes decrease. Characteristic gamma ray energies from a variety of elements are collected near the surface with a germanium detector. Of these, the 2.224 MeV gamma ray from hydrogen is sensitive to changes in soil organic carbon as low as 0.12% after counting for the equivalent of 3.45 days. Counting longer is recommended to reduce the sensitivity of the primary 4.438 MeV gamma ray from carbon below its current value of 2.81% in the simulation.
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Lanthanum Affects Bell Pepper Seedling Quality Depending on the Genotype and Time of Exposure by Differentially Modifying Plant Height, Stem Diameter and Concentrations of Chlorophylls, Sugars, Amino Acids, and Proteins
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Instrumental neutron activation analysis, gamma spectrometry and geographic information system techniques in the determination and mapping of rare earth element in phosphogypsum stacks
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Phosphogypsum is a by-product from the phosphate fertilizer industry, disposed in huge stacks in open-air storage areas. Its use in agriculture may be a solution to decrease these stacks, because, among its other uses, phosphogypsum can be used as a soil amendment to provide calcium and sulphur for major crops. However, it contains rare earth elements (REE) from its raw material. The objective of this study was to determine the concentrations of REE in phosphogypsum stacks Imbituba (southern Brazil) in order to verify the possibility of contamination in the surrounding of the stacks due to the disposal and to ensure the safe use of phosphogypsum in agriculture. Samples of phosphogypsum were collected and REE were determined by neutron activation analysis and gamma spectrometry. There was no leaching of the REE through the profile of the stacks, which suggests that the occurrence of REE in the phosphogypsum is associated with the formation of sulphates, carbonates, fluorides and phosphates. The results indicate that application of phosphogypsum from Imbituba to agricultural soils can contribute to increase the concentration of rare earth elements in the cultivated soils, but these are not available to plant uptake.
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Rare Earth Element Transfer from Soil to Navel Orange Pulp (Citrus sinensis Osbeck cv. Newhall) and the Effects on Internal Fruit Quality
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The effects of soil rare earth element (REE) on navel orange quality and safety in rare earth ore areas have gained great attention. This study investigated the transfer characteristics of REE from soil to navel orange pulp (Citrus sinensis Osbeck cv. Newhall) and examined the effects of soil REE on internal fruit quality in Xinfeng County, Jiangxi province, China. Path analysis showed that soil REE, pH, cation exchange capacity (CEC), and Fe oxide (Feox) significantly affected pulp REE concentrations. A Freundlich-type prediction model for pulp REE was established: log[REEpulp] = -1.036 + 0.272 log[REEsoil] - 0.056 pH - 0.360 log[CEC] + 0.370 log[Feox] (n = 114, R2 = 0.60). From the prediction model, it was inferred that even when soil REE and Feox were as high as 1038 mg kg-1 and 96.4 g kg-1, respectively, and pH and CEC were as low as 3.75 and 5.08 cmol kg-1, respectively, pulp REE concentrations were much lower than the food limit standard. Additionally, soil REE levels were significantly correlated with selected fruit quality indicators, including titratable acidity (r = 0.52, P < 0.01), total soluble solids (r = 0.48, P < 0.01) and vitamin C (r = 0.56, P < 0.01). Generally, under routine methods of water and fertilization management, the cultivation of navel oranges in rare earth ore areas of south China with soil REE ranging from 38.6 to 546 mg kg-1 had improved in internal fruit quality.
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Effects of rare earth elements on growth and metabolism of medicinal plants
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Full-text available
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The rare earth elements (REEs) are a set of 17 chemical elements. They include the lanthanide series from lanthanum (La) to lutetium (Lu), scandium (Sc), and yttrium (Y) in the periodic table. Although REEs are used widely in industry and agriculture in China for a long time, there has been increasing interest in application of REEs to medicinal plants in recent years. In this paper, we summarize researches in the past few decades regarding the effects of REEs on the germination of seeds, the growth of roots, total biomass, and the production of its secondary metabolites, as well as their effects on the absorption of minerals and metals by medicinal plants. By compilation and analysis of these data, we found that REEs have promoting effects at low concentrations and negative effects at comparatively high concentrations. However, most studies focused only on a few REEs, i.e., La, cerium (Ce), neodymium (Nd) and europium (Eu), and they made main emphasis on their effects on regulation of secondary metabolism in tissue-cultured plants, rather than cultivated medicinal plants. Advanced research should be invested regarding on the effects of REEs on yields of cultivated plants, specifically medicinal plants.
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Transfer of rare earth elements (REE) from natural soil to plant systems: Implications for the environmental availability of anthropogenic REE
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Full-text available
  • May 2012
Background and aims Rare Earth Elements (REE) are widely used to trace natural geochemical processes. They are also increasingly used by man (electronics industry, medicine, agriculture) and therefore considered as emerging pollutants. The present study documents REE mobility in non-polluted natural soil-plant systems in order to characterize their environmental availability for future anthropogenic pollution. Methods The study is based on a field approach in non-polluted natural sites with contrasting geological environments (limestone, granite, and carbonatite) and highly variable REE contents. Results REE concentrations in soils do not directly reflect bedrock concentrations, but depend largely on pedogenetic processes and on the mineralogy of bedrock and soil. The soils of all sites are with respect to bedrock enriched in heavy REE. The REE uptake by plants is not primarily controlled by the plant itself, but depends on the concentration and the speciation in the soil and the adsorbed soil water pool. Conclusions REE uptake by plant roots are linked with those of Fe. Roots absorb preferentially the light REE. Before translocation, REE are retained by the Casparian strip leading to much lower concentrations in the aerial parts. The transport of the REE within the xylem is associated with the general nutrient flux.
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Phosphorus (P) for Citrus Trees
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Phosphorus deficiency is not common in Florida citrus groves. If it does occur, it is more difficult to diagnose than nitrogen (N) deficiency or other nutrient element deficiencies. Growth is reduced when P supply is too low. Phosphorus is highly mobile in plants, so when it is deficient, it may move from old leaves to young leaves and other actively growing areas where energy is needed to form seeds and fruit. This 4-page fact sheet was written by Mongi Zekri and Tom Obreza and published by the UF Department of Soil and Water Science, July 2013. http://edis.ifas.ufl.edu/ss581
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The Rare-earth Metallome of Pecan and Other Carya
Article
  • Nov 2011
We report the composition of the rare-earth (REE) metallome component of the foliar ionomes of pecan (Carya illinoinensis) and other North American Carya and how accumulation of specific REEs relate to ploidy level and to accumulation of essential divalent nutrient elements. REE accumulation within the foliar ionomes of 12 Carya species, growing on a common site and soil, indicates that REEs accumulate according to the Oddo-Harkins rule with Ce, La, Nd, and Y (Ce > La > Nd > Y) being the dominant REEs with accumulated concentration typically being La > Ce > Nd > Y > Gd > Pr > Sm > Dy > Er > Yb > Ho > Tb >Tm > Sc >Lu. Carya species quantitatively differ in accumulation of REEs with all but C. aquatica accumulating at much greater concentrations than non-Carya tree species and with tetraploid Carya accumulating to approximately twice the concentration as diploid Carya. Carya tomentosa was an especially heavy accumulator of REEs at 859 μg·g -1 dry weight, whereas C. aquatica was especially light at 84 μg·g -1. Accumulation of REEs was such that any one element within this elemental class was tightly linked (generally r ≥ 0.94, but 0.81 for Ce) to all others. Accumulation of REEs is negatively correlated with Ca accumulation and positively correlated with Mn and Cu accumulation in diploid Carya. In tetraploid Carya, accumulated Mg, Ca, and Fe is positively associated with foliar concentration of REEs. Total concentration of REEs in pecan's foliar ionome was 190 μg·g -1, about equivalent to that of Mn. Circumstantial evidence suggests that one or more of the physiochemically similar REEs increases physiological plasticity and subsequent adaptive fitness to certain Carya species, especially tetraploids. Because all tetraploid Carya are high REE accumulators and are native to more xeric habitats than diploids, which typically occupy mesic habitats, it appears that REEs might play a role in Carya speciation and adaptation to certain site-limiting environmental stresses. REEs appear to play an unknown metabolic/ physiological role in pecan and most Carya species, especially tetraploids; thus, their nutritional physiology merits further investigation.
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Survey of lanthanoids in plants from a tropical region
Article
  • Apr 2011
Several anthropogenic sources may provide lanthanoids (La, Ce, Nd, Sm, Eu, Tb and Yb) to the agricultural and forestry landscapes. Because little information is available on the distribution of these chemical elements in Brazilian tropical ecosystems, this work focuses on the survey in leaves of diverse plant species (native trees, epiphytes and crops) from different ecosystems. Soil under crown projection was also analysed, thereby estimating the influence of its chemical composition on accumulation in leaves. The degree of lanthanoids accumulation varied substantially even for species growing in the same habitat. The most accumulator species, Alsophila sternbergii, presented the typical distribution pattern for lanthanoids, different from Pachystroma longifolium, a native species from the urban fragment, and the cultivated Citrus sp., in which the altered patterns revealed lanthanum enrichment in spite of cerium depletion in the leaves.
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