Ultrastructure and subcellular distribution of Cr in Iris pseudacorus L. using TEM and X-ray microanalysis
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Abstract
Chromium pollution of freshwater is hazardous for humans and other organisms, and places a limitation on the use of polluted water sources. Phytoremediation, the use of plants to remove pollutants from the environment, is a cost-effective, environmentally friendly approach for water decontamination. To improve the efficiency of the process, it is essential to increase the current knowledge about Cr accumulation in macrophytes. Plants of Iris pseudacorus L. were treated with Cr(III) at 0.75 mM for 5 weeks to investigate Cr localization by means of transmission electron microscopy and energy dispersive X-ray analysis. Chromium induced severe ultrastructural alterations in the rhizodermis (cell wall disorganisation, thickening, plasmolysis, and electron-dense inclusions) and rhizome parenchyma (reduced cell size, cell wall detachment, vacuolation, and opaque granules). The highest Cr contents were found in the cell walls of the cortex in the roots and in the cytoplasm and intercellular spaces of the rhizome. The Cr concentration in root tissues was in the order cortex >rhizodermis >stele, whereas in the rhizome, Cr was evenly distributed. It is proposed that root and rhizome have distinct functions in the response of I. pseudacorus to Cr. The rhizodermis limits Cr uptake by means of Si deposition and cell wall thickening. The rhizome cortex generates vacuoles and granules where Cr co-occurs with S, indicating Cr sequestration by metal-binding proteins.
Keywords
Chromium Metal Rhizome Subcellular localization Ultrastructure X-ray microanalysisAbbreviations
- EDX
Energy dispersive X-ray analysis
- PC
Phytochelatins
- TEM
Transmission electron microscopy
- USEPA
United States Environmental Protection Agency
Notes
Acknowledgments
This study was part of the International Cooperation European Project MEDINDUS, EC contract no INCO-CT-2004-509159. TEM and LM images were obtained in the TEM Laboratory of the University of Barcelona. X-ray microanalysis was performed in the Microscopy Service of the Autonomous University of Barcelona.
References
- Appenroth KJ, Stockel J, Srivastava A, Strasser RJ. Multiple effects of chromate on the photosynthetic apparatus of Spirodela polyrhiza as probed by OJIP chlorophyll a fluorescence measurements. Environ Pollut. 2001;115:49–64.PubMedCrossRefGoogle Scholar
- Barceló J, Poschenrieder C, Gunse B. Effect of chromium-VI on mineral element composition of bush beans. J Plant Nutr. 1985;8:211–7.CrossRefGoogle Scholar
- Barnhart J. Occurrences, uses, and properties of chromium. Regul Toxicol Pharmacol. 1997;26:S3–7.CrossRefGoogle Scholar
- Bluskov S, Arocena JM, Omotoso OO, Young JP. Uptake, distribution, and speciation of chromium in Brassica juncea. Int J Phytorem. 2005;7:153–65.CrossRefGoogle Scholar
- Bringezu K, Lichtenberger O, Leopold I, Neumann D. Heavy metal tolerance of Silene vulgaris. J Plant Physiol. 1999;154:536–46.Google Scholar
- Britez RM, Watanabe T, Jansen S, Reissmann CB, Osaki M. The relationship between aluminium and silicon accumulation in leaves of Faramea marginata (Rubiaceae). New Phytol. 2002;156:437–44.CrossRefGoogle Scholar
- Calheiros C, Rangel A, Castro P. The effects of tannery wastewater on the development of different plant species and chromium accumulation in Phragmites australis. Arch Environ Cont Toxicol. 2008;55:404–14.CrossRefGoogle Scholar
- Clemens S. Molecular mechanisms of plant metal tolerance and homeostasis. Planta. 2001;212:475–86.PubMedCrossRefGoogle Scholar
- Cobbett C, Goldsbrough P. Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Ann Rev Plant Biol. 2002;53:159–82.CrossRefGoogle Scholar
- Davies FT, Puryear JD, Newton RJ, Egilla JN, Grossi JAS. Mycorrhizal fungi increase chromium uptake by sunflower plants: influence on tissue mineral concentration, growth, and gas exchange. J Plant Nutr. 2002;25:2389–407.CrossRefGoogle Scholar
- Diwan H, Khan I, Ahmad A, Iqbal M. Induction of phytochelatins and antioxidant defence system in Brassica juncea and Vigna radiata in response to chromium treatments. Plant Growth Reg. 2010;61:97–107.CrossRefGoogle Scholar
- Duman F, Cicek M, Sezen G. Seasonal changes of metal accumulation and distribution in common club rush (Schoenoplectus lacustris) and common reed (Phragmites australis). Ecotoxicology. 2007;16:457–63.PubMedCrossRefGoogle Scholar
- Elangovan R, Philip L, Chandraraj K. Biosorption of chromium species by aquatic weeds: kinetics and mechanism studies. J Hazard Mater. 2008;152:100–12.PubMedCrossRefGoogle Scholar
- Gupta M, Rai UN, Tripathi RD, Chandra P. Lead-induced changes in glutathione and phytochelatin in Hydrilla verticillata (If) Royle. Chemosphere. 1995;30:2011–20.CrossRefGoogle Scholar
- Iglesia-Turiño S, Febrero A, Jauregui O, Caldelas C, Araus JL, Bort J. Detection and quantification of unbound phytochelatin 2 in plant extracts of Brassica napus grown with different levels of mercury. Plant Physiol. 2006;142:742–9.PubMedCrossRefGoogle Scholar
- Kotaś J, Stasicka Z. Chromium occurrence in the environment and methods of its speciation. Environ Pollut. 2000;107:263–83.PubMedCrossRefGoogle Scholar
- Krzesłowska M. The cell wall in plant cell response to trace metals: polysaccharide remodelling and its role in defence strategy. Act Physiol Plant. 2010;33(1):35–51.CrossRefGoogle Scholar
- Kumar AR, Riyazuddin P. Chromium speciation in a contaminated groundwater: redox processes and temporal variability. Environ Monit Assess. 2011;176:647–62.PubMedCrossRefGoogle Scholar
- Labra M, Gianazza E, Waitt R, Eberini I, Sozzi A, Regondi S, et al. Zea mays L. protein changes in response to potassium dichromate treatments. Chemosphere. 2006;62:1234–44.PubMedCrossRefGoogle Scholar
- Lahouti M, Jamshidi S, Ejtehadi H, Rowshani M, Mahmoodzadeh H. X-ray microanalysis and ultrastructural localization of chromium in Raphanus sativus L. Int J Bot. 2008;4:340–3.CrossRefGoogle Scholar
- Leita L, Contin M, Maggioni A. Distribution of cadmium and induced Cd-binding proteins in roots, stems and leaves of Phaseolus vulgaris. Plant Sci. 1991;77:139–47.CrossRefGoogle Scholar
- Liang YC, Sun WC, Zhu YG, Christie P. Mechanisms of silicon-mediated alleviation of abiotic stresses in higher plants: a review. Environ Pollut. 2007;147:422–8.PubMedCrossRefGoogle Scholar
- Liu D, Kottke I. Subcellular localization of chromium and nickel in root cells of Allium cepa by EELS and ESI. Cell Biol Toxicol. 2003;19:299–311.PubMedCrossRefGoogle Scholar
- Liu J, Duan CQ, Zhang XH, Zhu YN, Hu C. Subcellular distribution of chromium in accumulating plant Leersia hexandra Swartz. Plant Soil. 2009;322:187–95.CrossRefGoogle Scholar
- Mangabeira PA, Mielke MS, Arantes I, Dutruch L, Silva DD, Barbier F, et al. Bioaccumulation of chromium in aquatic macrophyte Borreria scabiosoides Cham. & Schltdl. Appl Surface Sci. 2006;252:6816–9.CrossRefGoogle Scholar
- Marchand L, Mench M, Jacob DL, Otte ML. Metal and metalloid removal in constructed wetlands, with emphasis on the importance of plants and standardized measurements: a review. Environ Pollut. 2010;158:3447–61.PubMedCrossRefGoogle Scholar
- Muramoto S, Aoyama I, Oki Y. Effect of salinity on the concentration of some elements in water hyacinth (Eichhornia crassipes) at critical levels. J Environ Sci Heal A. 1991;26:205–15.CrossRefGoogle Scholar
- Neumann D, zur Nieden U. Silicon and heavy metal tolerance of higher plants. Phytochemistry. 2001;56:685–92.PubMedCrossRefGoogle Scholar
- Paiva L, Oliveira J, Azevedo R, Ribeiro D, Silva M, Vitoria A. Ecophysiological responses of water hyacinth exposed to Cr3+ and Cr6+. Environ Exp Bot. 2009;65:403–9.CrossRefGoogle Scholar
- Park D, Yun YS, Jo JH, Park JM. Biosorption process for treatment of electroplating wastewater containing Cr(VI): laboratory-scale feasibility test. Ind Eng Chem Res. 2006;45:5059–65.CrossRefGoogle Scholar
- Peralta JR, Gardea-Torresdey JL, Tiemann KJ, Gómez E, Arteaga S, Rascon E, et al. Uptake and effects of five heavy metals on seed germination and plant growth in alfalfa (Medicago sativa L). Bull Environ Cont Toxicol. 2001;66:727–34.Google Scholar
- Pilon-Smits E. Phytoremediation. Annu Rev Plant Biol. 2005;56:15–39.PubMedCrossRefGoogle Scholar
- Probst A, Liu HY, Fanjul M, Liao B, Hollande E. Response of Vicia faba L. to metal toxicity on mine tailing substrate: geochemical and morphological changes in leaf and root. Environ Exp Bot. 2009;66:297–308.CrossRefGoogle Scholar
- Qiu S, Huang S. Study on growth and Cd accumulation of root system of Iris pseudacorus seedling under Cd stress. J Plant Res Environ. 2008;17:33–8.Google Scholar
- Rabier J, Laffont-Schwob I, Notonier R, Fogliani B, Bouraima-Madjebi S. Anatomical element localization by EDXS in Grevillea exul var. exul under nickel stress. Environ Pollut. 2008;156:1156–63.PubMedCrossRefGoogle Scholar
- Rehman A. Heavy metals uptake by Euglena proxima isolated from tannery effluents and its potential use in wastewater treatment. Russ J Ecol. 2011;42:44–9.CrossRefGoogle Scholar
- Rodríguez-Llorente ID, Pérez-Palacios P, Doukkali B, Caviedes MA, Pajuelo E. Expression of the seed-specific metallothionein mt4a in plant vegetative tissues increases Cu and Zn tolerance. Plant Sci. 2010;178:327–32.CrossRefGoogle Scholar
- Roig N, Nadal M, Sierra J, Ginebreda A, Schuhmacher M, Domingo JL. Novel approach for assessing heavy metal pollution and ecotoxicological status of rivers by means of passive sampling methods. Environ Int. 2011;37:671–7.PubMedCrossRefGoogle Scholar
- Rowbotham AL, Levy LS, Shuker LK. Chromium in the environment: an evaluation of exposure of the UK general population and possible adverse health effects. J Toxicol Environ Health B Crit Rev. 2000;3:145–78.PubMedCrossRefGoogle Scholar
- Saha B, Orvig C. Biosorbents for hexavalent chromium elimination from industrial and municipal effluents. Coord Chem Rev. 2010;254:2959–72.CrossRefGoogle Scholar
- Salt DE, Blaylock M, Kumar NPBA, Dushenkov V, Ensley BD, Chet I, et al. Phytoremediation—a novel strategy for the removal of toxic metals from the environment using plants. Nat Biotechnol. 1995;13:468–74.CrossRefGoogle Scholar
- Samantaray S, Rout GR, Das P. Role of chromium on plant growth and metabolism. Acta Physiol Plant. 1998;20:201–12.CrossRefGoogle Scholar
- Sanità di Toppi LS, Fossati F, Musetti R, Mikerezi I, Favali MA. Effects of hexavalent chromium on maize, tomato, and cauliflower plants. J Plant Nutr. 2002;25:701–17.CrossRefGoogle Scholar
- Shan XQ, Wang HI, Zhang SZ, Zhou HF, Zheng Y, Yu H, et al. Accumulation and uptake of light rare earth elements in a hyperaccumulator Dicropteris dichotoma. Plant Sci. 2003;165:1343–53.CrossRefGoogle Scholar
- Shanker AK, Cervantes C, Loza-Tavera H, Avudainayagam S. Chromium toxicity in plants. Environ Int. 2005;31:739–53.PubMedCrossRefGoogle Scholar
- Skeffington RA, Shewry PR, Peterson PJ. Chromium uptake and transport in barley seedlings (Hordeum vulgare L.). Planta. 1976;132:209–14.CrossRefGoogle Scholar
- Turnau K, Henriques FS, Anielska T, Renker C, Buscot F. Metal uptake and detoxification mechanisms in Erica andevalensis growing in a pyrite mine tailing. Environ Exp Bot. 2007;61:117–23.CrossRefGoogle Scholar
- Vajpayee P, Sharma SC, Tripathi RD, Rai UN, Yunus M. Bioaccumulation of chromium and toxicity to photosynthetic pigments, nitrate reductase activity and protein content of Nelumbo nucifera Gaertn. Chemosphere. 1999;39:2159–69.CrossRefGoogle Scholar
- Vajpayee P, Rai UN, Ali MB, Tripathi RD, Yadav V, Sinha S, et al. Chromium-induced physiologic changes in Vallisneria spiralis L. and its role in phytoremediation of tannery effluent. Bull Environ Cont Toxicol. 2001;67:246–56.Google Scholar
- Van Belleghem F, Cuypers A, Semane B, Smeets K, Vangronsveld J, d’Haen J, et al. Subcellular localization of cadmium in roots and leaves of Arabidopsis thaliana. New Phytol. 2007;173:495–508.PubMedCrossRefGoogle Scholar
- Vinodhini V, Das N. Packed bed column studies on Cr (VI) removal from tannery wastewater by neem sawdust. Desalination. 2010;264:9–14.CrossRefGoogle Scholar
- Wierzbicka MH, Przedpełska E, Ruzik R, Ouerdane L, Połeć-Pawlak K, Jarosz M, et al. Comparison of the toxicity and distribution of cadmium and lead in plant cells. Protoplasma. 2007;231:99–111.PubMedCrossRefGoogle Scholar
- Yang HJ, Shen ZM, Zhu SH, Wang WH. Heavy metals in wetland plants and soil of Lake Taihu, China. Environ Toxicol Chem. 2008;27:38–42.PubMedCrossRefGoogle Scholar
- Yılmaz S, Türe M, Sadıkoglu M, Duran A. Determination of total Cr in wastewaters of Cr electroplating factories in the I.organize industry region (Kayseri, Turkey) by ICP-AES. Environ Monit Assess. 2010;167:235–42.PubMedCrossRefGoogle Scholar
- Zargar SM, Nazir M, Agrawal GK, Kim DW, Rakwal R. Silicon in plant tolerance against environmental stressors: towards crop improvement using omics approaches. Curr Prot. 2010;7:135–43.CrossRefGoogle Scholar
- Zhang XB, Liu P, Yang YS, Chen WR. Phytoremediation of urban wastewater by model wetlands with ornamental hydrophytes. J Environ Sci. 2007;19:902–9.CrossRefGoogle Scholar
- Zhitkovich A. Importance of chromium-DNA adducts in mutagenicity and toxicity of chromium(VI). Chem Res Toxicol. 2005;18:3–11.PubMedCrossRefGoogle Scholar
- Zhou YQ, Huang SZ, Yu SL, Gu JG, Zhao JZ, Han YL, et al. The physiological response and sub-cellular localization of lead and cadmium in Iris pseudacorus L. Ecotoxicol. 2010;19:69–76.CrossRefGoogle Scholar