Abstract
Background and aim
Iron plaque at the soil-root interface is a key position for uptake of heavy metals by plants. Exploring iron plaque’s role in Pb uptake by edible vegetable roots aids understanding Pb uptake mechanisms and developing methods to reduce Pb accumulation.
Methods
Soil and plant Pb contents were determined. Micro X-ray fluorescence (micro-XRF) determined Fe and Pb distributions in waterlogged and terrestrial Oenanthe javanica DC. roots, and X-ray absorption near-edge spectroscopy (XANES) identified Pb speciation in bulk soil, rhizosphere soil and plant tissues.
Results
Waterlogged O. javanica accumulated more Pb and exhibited a higher Pb transfer factor than terrestrial O. javanica. In waterlogged O. javanica, the iron plaque and epidermis contained the most Fe, while the root vasculature contained the most Pb. In terrestrial O. javanica roots, Fe and Pb had similar distributions. Bulk and rhizosphere soils contained different Pb species, and rhizosphere soil had Pb-humate. For iron plaque, a new Pb complex, Pb-ferrihydrite, was identified. Biologically important groups bound (-S, -COO) and precipitated (-PO4) Pb were identified in plants.
Conclusions
Waterlogged O. javanica root iron plaque and humic acid increase Pb uptake and accumulation. Thus, avoiding O. javanica root iron plaque formation (dry land growth) and growing in low-humic soil reduce Pb uptake and entry into the food chain.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Abbreviations
- DCB:
-
dithionite-citrate-bicarbonate
- micro-XRF:
-
micro X-ray fluorescence
- XAS:
-
X-ray absorption spectroscopy
- XANES:
-
X-ray absorption near-edge spectroscopy
- EXAFS:
-
Extended X-ray absorption fine structure spectroscopy
- LMWOAs:
-
low-molecular-weight organic acids
- XRF:
-
X-ray fluorescence
- SSRF:
-
Shanghai Synchrotron Radiation Facility
- ICP-MS:
-
inductively coupled plasma mass spectrometry
- ICP-OES:
-
inductively coupled plasma optical emission spectroscopy
- HA:
-
humic acid
- HNS:
-
Hoagland’s nutrient solution
References
Amaral DC, Lopes G, Guilherme LRG, Seyfferth AL (2017) A new approach to sampling intact Fe plaque reveals Si-induced changes in Fe mineral composition and shoot as in rice. Environ Sci Technol 51:38–45. https://doi.org/10.1021/acs.est.6b03558
And ME, ValsamiJones É, Cotterhowells JD (2000) Bonemeal additions as a remediation treatment for metal contaminated soil. Environ Sci Technol 34:3501–3507. https://doi.org/10.1021/es990972a
Andra SS, Datta R, Sarkar D, Makris KC, Mullens CP, Sahi SV, Bach SBH (2010) Synthesis of phytochelatins in vetiver grass upon lead exposure in the presence of phosphorus. Plant Soil 326:171–185. https://doi.org/10.1007/s11104-009-9992-2
Bendebane S, Tifouti L, Djerad S (2016) The effect of the nature of organic acids and the hydrodynamic conditions on the dissolution of Pb particles. RSC Adv 7:77–86. https://doi.org/10.1039/c6ra24777f
Blute NK, Brabander DJ, Hemond HF, Sutton SR, Newville MG, Rivers ML (2004) Arsenic sequestration by ferric iron plaque on cattail roots. Environ Sci Technol 38:6074–6077. https://doi.org/10.1021/es049448g
Bovenkamp GL, Prange A, Schumacher W, Ham K, Smith AP, Hormes J (2013) Lead uptake in diverse plant families: a study applying X-ray absorption near edge spectroscopy. Environ Sci Technol 47:4375–4382. https://doi.org/10.1021/es302408m
Chen B, Zhu YG (2006) Humic acids increase the phytoavailability of cd and Pb to wheat plants cultivated in freshly spiked, contaminated soil. J Soils Sediments 6:236–242. https://doi.org/10.1065/jss2006.08.178
Chen Z, Zhu YG, Wen JL, Meharg AA (2005) Direct evidence showing the effect of root surface iron plaque on arsenite and arsenate uptake into rice (Oryza sativa) roots. New Phytol 165:91–97. https://doi.org/10.1111/j.1469-8137.2004.01241.x
Cheng H, Wang M, Ming HW, Ye Z (2014) Does radial oxygen loss and iron plaque formation on roots alter cd and Pb uptake and distribution in rice plant tissues? Plant Soil 375:137–148. https://doi.org/10.1007/s11104-013-1945-0
Du HH, Huang QY, Lei M, Tie BQ (2018) Sorption of Pb(II) by nanosized ferrihydrite organo-mineral composites formed by adsorption versus coprecipitation. ACS Earth Space Chem 2:556–564. https://doi.org/10.1021/acsearthspacechem.8b00005
Duan DC, Peng C, Xu C, Yu MG, Sun LJ, Worden N, Shi JY, Hu TD (2014) Lead phytoavailability change driven by its speciation transformation after the addition of tea polyphenols (TPs): combined selective sequential extraction (SSE) and XANES analysis. Plant Soil 382:103–115. https://doi.org/10.1007/s11104-014-2152-3
Evangelou MW, Daghan H, Schaeffer A (2004) The influence of humic acids on the phytoextraction of cadmium from soil. Chemosphere 57:207–213. https://doi.org/10.1016/j.chemosphere.2004.06.017
Evangelou MW, Ebel M, Schaeffer A (2006) Evaluation of the effect of small organic acids on phytoextraction of cu and Pb from soil with tobacco Nicotiana tabacum. Chemosphere 63:996–1004. https://doi.org/10.1016/j.chemosphere.2005.08.042
Fischer S, Kuhnlenz T, Thieme M, Schmidt H, Clemens S (2014) Analysis of plant Pb tolerance at realistic submicromolar concentrations demonstrates the role of phytochelatin synthesis for Pb detoxification. Environ Sci Technol 48:7552–7559. https://doi.org/10.1021/es405234p
Gaur A, Shrivastava BD (2012) A comparative study of the methods of speciation using X-ray absorption fine structure. Acta Phys Pol A 121:647–652. https://doi.org/10.12693/aphyspola.121.647
GB15618-2008 (2008) Environmental quality standard for soils. General administration of Environmental Protection and General administration of quality supervision, inspection and quarantine, China, Beijing
GB2762-2012 (2012) Maximum levels of contaminants in foods vol GB2762-2012
Guo JX, Li YY, Hu C, Zhou S, Xu H, Zhang QJ, Wang G (2018) Ca-containing amendments to reduce the absorption and translocation of Pb in rice plants. Sci Total Environ 637:971–979. https://doi.org/10.1016/j.scitotenv.2018.05.100
Hansel CM, Fendorf S, Sutton S, Newville M (2001) Characterization of Fe plaque and associated metals on the roots of mine-waste impacted aquatic plants. Environ Sci Technol 35:3863–3868. https://doi.org/10.1021/es0105459
Hansel CM, La Force MJ, Fendorf S, Sutton S (2002) Spatial and temporal association of as and Fe species on aquatic plant roots. Environ Sci Technol 36:1988–1994. https://doi.org/10.1021/es015647d
Herndon EM, Martínez CE, Brantley SL (2014) Spectroscopic (XANES/XRF) characterization of contaminant manganese cycling in a temperate watershed. Biogeochemistry 121:505–517. https://doi.org/10.1007/s10533-014-0018-7
Huang QQ, Wang Q, Luo Z, Yu Y, Jiang RF, Li HF (2015) Effects of root iron plaque on selenite and selenate dynamics in rhizosphere and uptake by rice (Oryza sativa). Plant Soil 388:255–266. https://doi.org/10.1007/s11104-014-2329-9
Huang L, Zhang HQ, Song YY, Yang YR, Chen H, Tang M (2017) Subcellular compartmentalization and chemical forms of lead participate in lead tolerance of Robinia pseudoacacia L. with Funneliformis mosseae. Front Plant Sci 8. https://doi.org/10.3389/fpls.2017.00517
Ji Y, Vollenweider P, Lenz M, Schulin R, Tandy S (2018) Can iron plaque affect Sb(III) and Sb(V) uptake by plants under hydroponic conditions. Environ Exp Bot 148:168–175. https://doi.org/10.1016/j.envexpbot.2018.01.014
Khan N, Seshadri B, Bolan N, Saint CP, Kirkham MB, Chowdhury S, Yamaguchi N, Lee DY, Li G, Kunhikrishnan A, Qi F, Karunanithi R, Qiu R, Zhu YG, Syu CH (2016) Root iron plaque on wetland plants as a dynamic pool of nutrients and contaminants. Adv Agron 138:1–96. https://doi.org/10.1016/bs.agron.2016.04.002
Kwonrae K, Owens G, Naidu R, Soonlk K (2010) Influence of plant roots on rhizosphere soil solution composition of long-term contaminated soils. Geoderma 155:86–92. https://doi.org/10.1016/j.geoderma.2009.11.028
Li X, Bu N, Li Y, Ma L, Xin S, Zhang L (2012) Growth, photosynthesis and antioxidant responses of endophyte infected and non-infected rice under lead stress conditions. J Hazard Mater 213–214:55–61. https://doi.org/10.1016/j.jhazmat.2012.01.052
Li FL, Yang CM, Syu CH, Lee DY, Tsuang BJ, Juang KW (2015) Combined effect of rice genotypes and soil characteristics on iron plaque formation related to Pb uptake by rice in paddy soils. J Soils Sediments 16:1–9. https://doi.org/10.1007/s11368-015-1169-4
Liu WJ, Zhu YG, Hu Y, Williams PN, Gault AG, Meharg AA, Charnock JM, Smith FA (2006) Arsenic sequestration in iron plaque, its accumulation and speciation in mature rice plants (Oryza Sativa L.). Environ Sci Technol 40:5730–5736. https://doi.org/10.1021/es060800v
Liu HJ, Zhang JL, Christie P, Zhang FS (2008) Influence of iron plaque on uptake and accumulation of cd by rice (Oryza sativa L.) seedlings grown in soil. Sci Total Environ 394:361–368. https://doi.org/10.1016/j.scitotenv.2008.02.004
Liu JG, Leng XM, Wang MX, Zhu ZZ, Dai QH (2011) Iron plaque formation on roots of different rice cultivars and the relation with lead uptake. Ecotoxicol Environ Saf 74:1304–1309. https://doi.org/10.1016/j.ecoenv.2011.01.017
Liu CY, Gong XF, Chen CL, Yang JY, Xu S (2016) The effect of iron plaque on lead translocation in soil-Carex cinerascens kukenth. system. Int J Phytorem 18:1–9. https://doi.org/10.1080/15226514.2015.1021954
Luo LQ, Chu BB, Liu Y, Wang XF, Xu T, Bo Y (2014) Distribution, origin, and transformation of metal and metalloid pollution in vegetable fields, irrigation water, and aerosols near a Pb-Zn mine. Environ Sci Pollut R 21:8242–8260. https://doi.org/10.1007/s11356-014-2744-8
Luo LQ, Shen YT, Liu J, Zeng Y (2016) Investigation of Pb species in soils, celery and duckweed by synchrotron radiation X-ray absorption near-edge structure spectrometry. Spectrochim Acta B At Spectrosc 122:40–45. https://doi.org/10.1016/j.sab.2016.05.017
Luo Q, Wang S, Sun LN, Wang H (2017) Metabolic profiling of root exudates from two ecotypes of Sedum alfredii treated with Pb based on GC-MS. Sci Rep 7:39878. https://doi.org/10.1038/srep39878
Martin M, Violante A, Ajmone-Marsan F, Barberis E (2014) Surface interactions of arsenite and arsenate on soil colloids. Soil Sci Soc Am J 78:157–170. https://doi.org/10.2136/sssaj2013.04.0133
Niazi NK, Singh B, Shah P (2011) Arsenic speciation and phytoavailability in contaminated soils using a sequential extraction procedure and XANES spectroscopy. Environ Sci Technol 45:7135–7142. https://doi.org/10.1021/es201677z
Nordhei C, Mathisen K, Safonova O, van Beek W, Nicholson DG (2009) Decomposition of carbon dioxide at 500 °C over reduced iron, cobalt, nickel, and zinc ferrites: a combined XANES-XRD study. J Phys Chem C 113:19568–19577. https://doi.org/10.1021/jp9049473
Otte M, Dekkers I, Rozema J, Broekman R (1991) Uptake of arsenic by Aster tripolium in relation to rhizosphere oxidation. Can J Bot 69:2670–2677. https://doi.org/10.1139/b91-335
Peralta-Videa JR, Lopez ML, Narayan M, Saupe G, Gardea-Torresdey J (2009) The biochemistry of environmental heavy metal uptake by plants: Implications for the food chain. Int J Biochem Cell Biol 41:1665–1677. https://doi.org/10.1016/j.biocel.2009.03.005
Pi N, Tam NFY, Wong MH (2011) Formation of iron plaque on mangrove roots receiving wastewater and its role in immobilization of wastewater-borne pollutants. Mar Pollut Bull 63:402–411. https://doi.org/10.1016/j.marpolbul.2011.05.036
Qian Y, Feng H, Gallagher FJ, Zhu Q, Wu M, Liu CJ, Jones KW, Tappero RV (2015) Synchrotron study of metal localization in Typha latifolia L. root sections. J Synchrotron Radiat 22:1459–1468. https://doi.org/10.1107/s1600577515017269
Qin F, Shan XQ, Wei B (2004) Effects of low-molecular-weight organic acids and residence time on desorption of cu, cd, and Pb from soils. Chemosphere 57:253–263. https://doi.org/10.1016/j.chemosphere.2004.06.010
Sanderson P, Naidu R, Bolan N (2016) The effect of environmental conditions and soil physicochemistry on phosphate stabilisation of Pb in shooting range soils. J Environ Manag 170:123–130. https://doi.org/10.1016/j.jenvman.2016.01.017
Scheidegger C, Behra R, Sigg L (2011) Phytochelatin formation kinetics and toxic effects in the freshwater alga Chlamydomonas reinhardtii upon short- and long-term exposure to lead(II). Aquat Toxicol 101:423–429. https://doi.org/10.1016/j.aquatox.2010.11.016
Schreck E, Dappe V, Sarret G, Sobanska S, Nowak D, Nowak J, Stefaniak EA, Magnin V, Ranieri V, Dumat C (2014) Foliar or root exposures to smelter particles: consequences for lead compartmentalization and speciation in plant leaves. Sci Total Environ 476:667–676. https://doi.org/10.1016/j.scitotenv.2013.12.089
Shahid M, Pinelli E, Dumat C (2012) Review of Pb availability and toxicity to plants in relation with metal speciation; role of synthetic and natural organic ligands. J Hazard Mater 219-220:1–12. https://doi.org/10.1016/j.jhazmat.2012.01.060
Sharma P, Dubey RS (2005) Lead toxicity in plants. Braz J Plant Physiol 17:35–52. https://doi.org/10.1590/S1677-04202005000100004
Sharma NC, Gardea-Torresdey JL, Parsons J, Sahi SV (2004) Chemical speciation and cellular deposition of lead in Sesbania drummondii. Environ Toxicol Chem 23:2068–2073. https://doi.org/10.1897/03-540
Shen YT (2014) Distribution and speciation of lead in model plant Arabidopsis thaliana by synchrotron radiation X-ray fluorescence and absorption near edge structure spectrometry. X-Ray Spectrom 43:146–151. https://doi.org/10.1002/xrs.2531
Shen YT, Song YF (2017) Effects of organic ligands on Pb absorption and speciation changes in Arabidopsis as determined by micro X-ray fluorescence and X-ray absorption near-edge structure analysis. J Synchrotron Radiat 24:463–468. https://doi.org/10.1107/S1600577517001941
Shi W, Jin ZF, Hu SY, Fang XM, Li FL (2017) Dissolved organic matter affects the bioaccumulation of copper and lead in Chlorella pyrenoidosa: a case of long-term exposure. Chemosphere 174:447–455. https://doi.org/10.1016/j.chemosphere.2017.01.119
Sima JK, Cao XD, Zhao L, Luo QS (2015) Toxicity characteristic leaching procedure over- or under-estimates leachability of lead in phosphate-amended contaminated soils. Chemosphere 138:744–750. https://doi.org/10.1016/j.chemosphere.2015.07.028
Siqueira-Silva AI, da Silva LC, Azevedo AA, Oliva MA (2012) Iron plaque formation and morphoanatomy of roots from species of Restinga subjected to excess iron. Ecotoxicol Environ Saf 78:265–275. https://doi.org/10.1016/j.ecoenv.2011.11.030
Stewart TJ, Szlachetko J, Sigg L, Behra R, Nachtegaal M (2015) Tracking the temporal dynamics of intracellular lead speciation in a green alga. Environ Sci Technol 49:11176–11181. https://doi.org/10.1021/acs.est.5b02603
Sukreeyapongse O, Holm PE, Strobel BW, Panichsakpatana S, Magid J, Hansen HCB (2002) pH-dependent release of cadmium, copper, and lead from natural and sludge-amended soils. J Environ Qual 31:1901–1909. https://doi.org/10.2134/jeq2002.1901
Sun JL, Luo LQ (2014) A study on distribution and chemical speciation of lead in corn seed germination by synchrotron radiation X-ray fluorescence and absorption near edge structure spectrometry. Chin J Anal Chem 42:1447–1452. https://doi.org/10.2134/jeq2002.1901
Sun J, Mailloux BJ, Chillrud SN, van Geen A, Thompson A, Bostick BC (2018) Simultaneously quantifying ferrihydrite and goethite in natural sediments using the method of standard additions with X-ray absorption spectroscopy. Chem Geol 476:248–259. https://doi.org/10.1016/j.chemgeo.2017.11.021
Syu CH, Lee CH, Jiang PY, Chen MK, Lee DY (2014) Comparison of as sequestration in iron plaque and uptake by different genotypes of rice plants grown in as-contaminated paddy soils. Plant Soil 374:411–422. https://doi.org/10.1007/s11104-013-1893-8
Tripathi RD, Tripathi P, Dwivedi S, Kumar A, Mishra A, Chauhan PS, Norton GJ, Nautiyal CS (2014) Roles for root iron plaque in sequestration and uptake of heavy metals and metalloids in aquatic and wetland plants. Metallomics 6:1789–1800. https://doi.org/10.1039/c4mt00111g
Trivedi P, Dyer JA, Sparks DL (2003) Lead sorption onto ferrihydrite. 1. A macroscopic and spectroscopic assessment. Environ Sci Technol 37:908–914. https://doi.org/10.1021/es0257927
Wang HH, Shan XQ, Liu T, Xie YN, Wen B, Zhang SZ, Han F, van Genuchten MT (2007) Organic acids enhance the uptake of lead by wheat roots. Planta 225:1483–1494. https://doi.org/10.1007/s00425-006-0433-7
Wang M, Zhang Z, Ren J, Zhang C, Li CP, Guo GL, Li FS (2017) Microscopic evidence for humic acid induced changes in lead immobilization by phosphate in a counterdiffusion system. J Hazard Mater 330:46–51. https://doi.org/10.1016/j.jhazmat.2017.02.008
Xu Y, Sun XL, Zhang QQ, Li XZ, Yan ZZ (2018) Iron plaque formation and heavy metal uptake in Spartina alterniflora at different tidal levels and waterlogging conditions. Ecotoxicol Environ Saf 153:91–100. https://doi.org/10.1016/j.ecoenv.2018.02.008
Yamaguchi N, Ohkura T, Takahashi Y, Maejima Y, Arao T (2014) Arsenic distribution and speciation near rice roots influenced by iron plaques and redox conditions of the soil matrix. Environ Sci Technol 48:1549–1556. https://doi.org/10.1021/es402739a
Ye Z, Baker AJM, Wong MH, Willis AJ (1998) Zinc, lead and cadmium accumulation and tolerance in Typha latifolia as affected by iron plaque on the root surface. Aquat Bot 61:55–67. https://doi.org/10.1016/S0304-3770(98)00057-6
Ye XX, Li HY, Zhang LG, Chai RS, Tu RF, Gao HJ (2018) Amendment damages the function of continuous flooding in decreasing cd and Pb uptake by rice in acid paddy soil. Ecotoxicol Environ Saf 147:708–714. https://doi.org/10.1016/j.ecoenv.2017.09.034
Zeng GG, Wan J, Huang DL, Hu L, Huang C, Cheng M, Xue WJ, Gong XM, Wang RZ, Jiang DN (2017) Precipitation, adsorption and rhizosphere effect: the mechanisms for phosphate-induced Pb immobilization in soils—a review. J Hazard Mater 339:354–367. https://doi.org/10.1016/j.jhazmat.2017.05.038
Zhong SQ, Shi JC, Xu JM (2010) Influence of iron plaque on accumulation of lead by yellow flag (Iris pseudacorus L.) grown in artificial Pb-contaminated soil. J Soils Sediments 10:964–970. https://doi.org/10.1007/s11368-010-0213-7
Zhou XB, Shi WM, Zhang LH (2007) Iron plaque outside roots affects selenite uptake by rice seedlings (Oryza sativa L.) grown in solution culture. Plant Soil 290:17–28. https://doi.org/10.1007/s11104-006-9072-9
Acknowledgments
This work was supported by the National Key Research and Development Program of China (Grant No. 2016YFC0600603), the National Natural Science Foundation of China (Grant No. 20775018, 41877505 and 41201527), the National High Technology Research and Development Program of China (Grant No. 2007AA06Z124) and the Project of China Geological Survey (Grant No. DD20160340). The Shanghai Synchrotron Radiation Facility is thanked for provision of beam time at beamlines 15 U1 and 14 W1. In addition, we thank associate Professor Yating Shen, Dr. Yuan Zeng and Dr. Xiaoyan Sun for their technical support during the experiments and data collection.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Declarations of interest
None
Additional information
Responsible Editor: Antony Van der Ent.
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOCX 28.2 kb)
Rights and permissions
About this article
Cite this article
Liu, J., Luo, L. Uptake and transport of Pb across the iron plaque of waterlogged dropwort (Oenanthe javanica DC.) based on micro-XRF and XANES. Plant Soil 441, 191–205 (2019). https://doi.org/10.1007/s11104-019-04106-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-019-04106-w