Comparative analyses of cadmium and zinc uptake correlated with changes in natural resistance-associated macrophage protein (NRAMP) expression in Solanum nigrum L. and Brassica rapa
Y. Song A B , L. Hudek C , D. Freestone B , J. Puhui A , A. A. Michalczyk B , Z. Senlin A and M. L. Ackland B D
+ Author Affiliations
- Author Affiliations
A Key Laboratory of Pollution Ecology and Environmental Engineering, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang 110016, People’s Republic of China.
B School of Life and Environmental Sciences, Deakin University, Burwood, Vic. 3125 Australia.
C Centre for Regional and Rural Futures, Deakin University, Burwood, Vic. 3125, Australia.
D Corresponding author. Email: leigha@deakin.edu.au
Environmental Chemistry 11(6) 653-660 https://doi.org/10.1071/EN14078
Submitted: 14 April 2014 Accepted: 28 June 2014 Published: 5 November 2014
Environmental context. Soils contaminated with metals can pose both environmental and human health risks. This study showed that a common crop vegetable grown in the presence of cadmium and zinc readily accumulated these metals, and thus could be a source of toxicity when eaten. The work highlights potential health risks from consuming crops grown on contaminated soils.
Abstract. Ingestion of plants grown in heavy metal contaminated soils can cause toxicity because of metal accumulation. We compared Cd and Zn levels in Brassica rapa, a widely grown crop vegetable, with that of the hyperaccumulator Solanum nigrum L. Solanum nigrum contained 4 times more Zn and 12 times more Cd than B. rapa, relative to dry mass. In S. nigrum Cd and Zn preferentially accumulated in the roots whereas in B. rapa Cd and Zn were concentrated more in the shoots than in the roots. The different distribution of Cd and Zn in B. rapa and S. nigrum suggests the presence of distinct metal uptake mechanisms. We correlated plant metal content with the expression of a conserved putative natural resistance-associated macrophage protein (NRAMP) metal transporter in both plants. Treatment of both plants with either Cd or Zn increased expression of the NRAMP, with expression levels being higher in the roots than in the shoots. These findings provide insights into the molecular mechanisms of heavy metal processing by S. nigrum L. and the crop vegetable B. rapa that could assist in application of these plants for phytoremediation. These investigations also highlight potential health risks associated with the consumption of crops grown on contaminated soils.
Additional keywords: heavy metal, hyperaccumulator, natural resistance-associated macrophage protein (NRAMP) gene, soil contamination.
References
[1] J. O. Nriagu, J. M. Pacyna, Quantitative assessment of worldwide contamination of air, water and soils by trace metals. Nature 1988, 333, 134.| Quantitative assessment of worldwide contamination of air, water and soils by trace metals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXktFSqsrw%3D&md5=94c309a6c74919f4be65da901a4f3499CAS | 3285219PubMed |
[2] F. A. Sartor, D. J. Rondia, F. D. Claeys, J. A. Staessen, R. R. Lauwerys, A. M. Bernard, J. P. Buchet, H. A. Roels, P. J. Bruaux, G. M. Ducoffre, P. J. Lijnen, L. B. Thijs, A. K. Amery, Impact of environmental cadmium pollution on cadmium exposure and body burden. Arch. Environ. Health 1992, 47, 347.
| Impact of environmental cadmium pollution on cadmium exposure and body burden.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXis1Ohug%3D%3D&md5=b2eb30231e47e460a5a922ef5cfdbff5CAS | 1444596PubMed |
[3] S. P. McGrath, F. J. Zhao, Phytoextraction of metals and metalloids from contaminated soils. Curr. Opin. Biotechnol. 2003, 14, 277.
| Phytoextraction of metals and metalloids from contaminated soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXltVSqsrc%3D&md5=c125437f74a294937a64e7633c348e6dCAS | 12849780PubMed |
[4] A. J. M. Baker, S. P. McGrath, R. D. Reeves, J. A. C. Smith, Metal hyperaccumulator plants: a review of the ecology and physiology of a biochemical resource for phytoremediation of metal-polluted soils, in Phytoremediation of Contaminated Soil and Water (Eds N. Terry, G. Banuelos) 2000, pp. 85–107 (Lewis Publishers: Boca Raton, FL).
[5] J. F. Ma, D. Ueno, F. J. Zhao, S. P. McGrath, Subcellular localisation of Cd and Zn in the leaves of a Cd-hyperaccumulating ecotype of Thlaspi caerulescens. Planta 2005, 220, 731.
| Subcellular localisation of Cd and Zn in the leaves of a Cd-hyperaccumulating ecotype of Thlaspi caerulescens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhvVSqs7g%3D&md5=86e4a53c03b4a2c119ef86260273b996CAS | 15517354PubMed |
[6] M. M. Lasat, A. J. M. Baker, L. V. Kochian, Altered Zn compartmentation in the root symplasm and stimulated Zn absorption into the leaf as mechanisms involved in Zn hyperaccumulation in Thlaspi caerulescens.. Plant Physiol. 1998, 118, 875.
| Altered Zn compartmentation in the root symplasm and stimulated Zn absorption into the leaf as mechanisms involved in Zn hyperaccumulation in Thlaspi caerulescens..Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnsFekt7k%3D&md5=50a9f7b01485cd82595daf2e9084c832CAS | 9808732PubMed |
[7] S. L. Brown, R. L. Chaney, J. S. Angle, A. Baker, Zinc and cadmium uptake by hyperaccumulator Thlaspi caerulescens grown in nutrient solution. Soil Sci. Soc. Am. J. 1995, 59, 125.
| Zinc and cadmium uptake by hyperaccumulator Thlaspi caerulescens grown in nutrient solution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjtleltr0%3D&md5=c78c0e9a23a0c1307080b444d8539f2bCAS |
[8] E. Gérard, G. Echevarria, T. Sterckeman, J. L. Morel, Cadmium availibility to three plant species varying in cadmium accumulation pattern. J. Environ. Qual. 2000, 29, 1117.
| Cadmium availibility to three plant species varying in cadmium accumulation pattern.Crossref | GoogleScholarGoogle Scholar |
[9] H. Küpper, E. Lombi, F. J. Zhao, S. P. McGrath, Cellular compartmentation of cadmium and zinc in relation to other elements in the hyperaccumulator Arabidopsis halleri. Planta 2000, 212, 75.
| Cellular compartmentation of cadmium and zinc in relation to other elements in the hyperaccumulator Arabidopsis halleri.Crossref | GoogleScholarGoogle Scholar | 11219586PubMed |
[10] H. Küpper, A. Mijovilovich, W. Meyer-Klaucke, P. M. Kroneck, Tissue- and age-dependent differences in the complexation of cadmium and zinc in the cadmium/zinc hyperaccumulator Thlaspi caerulescens (Ganges ecotype) revealed by X-ray absorption spectroscopy. Plant Physiol. 2004, 134, 748.
| Tissue- and age-dependent differences in the complexation of cadmium and zinc in the cadmium/zinc hyperaccumulator Thlaspi caerulescens (Ganges ecotype) revealed by X-ray absorption spectroscopy.Crossref | GoogleScholarGoogle Scholar | 14966248PubMed |
[11] S. P. McGrath, E. Lombi, C. W. Gray, N. Caille, S. J. Dunham, F. J. Zhao, Field evaluation of Cd and Zn phytoextraction potential by the hyperaccumulators Thlaspi caerulescens and Arabidopsis halleric. Environ. Pollut. 2006, 141, 115.
| Field evaluation of Cd and Zn phytoextraction potential by the hyperaccumulators Thlaspi caerulescens and Arabidopsis halleric.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xis1Wgsbs%3D&md5=41a8f7f3c2fefc0f4b7425c9bb017ae2CAS | 16202493PubMed |
[12] D. Ueno, T. Iwashita, F. J. Zhao, J. F. Ma, Characterization of Cd translocation and identification of the Cd form in xylem sap of the Cd-hyperaccumulator Arabidopsis halleri. Plant Cell Physiol. 2008, 49, 540.
| Characterization of Cd translocation and identification of the Cd form in xylem sap of the Cd-hyperaccumulator Arabidopsis halleri.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmsVWntL0%3D&md5=71e0a96412157d14f020faf86e408944CAS | 18281325PubMed |
[13] F. J. Zhao, R. E. Hamon, E. Lombi, M. J. McLaughlin, S. P. McGrath, Characteristics of cadmium uptake in two contrasting ecotypes of the hyperaccumulator Thlaspi caerulescens. J. Experiment. Bot. 2002, 53, 535.
| Characteristics of cadmium uptake in two contrasting ecotypes of the hyperaccumulator Thlaspi caerulescens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XitVegtL8%3D&md5=beed825579f83712d00bd4432c353e88CAS |
[14] F. J. Zhao, R. F. Jiang, S. J. Dunham, S. P. McGrath, Cadmium uptake, translocation and tolerance in the hyperaccumulator Arabidopsis halleri. New Phytol. 2006, 172, 646.
| Cadmium uptake, translocation and tolerance in the hyperaccumulator Arabidopsis halleri.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlCjur%2FK&md5=8e183dd3fa37917cab6b0998bced6da0CAS | 17096791PubMed |
[15] C. W. A. do Nascimento, D. Amarasiriwardena, B. Xing, Comparison of natural organic acids and synthetics chelates at enhancing phytoextraction of metals from a multi-metal contaminated soil. Environ. Pollut. 2006, 140, 114.
| Comparison of natural organic acids and synthetics chelates at enhancing phytoextraction of metals from a multi-metal contaminated soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XitFKqtw%3D%3D&md5=cf8f164cb6f2557c4372afceecbc4e76CAS |
[16] W. A. Peer, I. R. Baxter, E. L. Richards, J. L. Freeman, A. S. Murphy, Phytoremediation and hyperaccumulator plants, in Molecular Biology of Metal Homeostasis and Detoxification (Eds M. J. Tamás, E. Martinoia) 2005, Vol. 232, pp. 207–214 (Springer: Heidelberg, Germany).
[17] S. P. McGrath, F. J. Zhao, E. Lombi, Plant and rhizosphere processes involved in phytoremediation of metal-contaminated soils. Plant Soil 2001, 232, 207.
| Plant and rhizosphere processes involved in phytoremediation of metal-contaminated soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsVCksLY%3D&md5=dd0225e49e75cd4c8968b77a3c7bc994CAS |
[18] R. L. Sun, Q. X. Zhou, F. H. Sun, C. X. Jin, Antioxidant defense and proline/phytochelatin accumulation in a newly discovered Cd-hyperaccumulator, Solanum nigrum L. Environ. Exp. Bot. 2007, 60, 468.
| Antioxidant defense and proline/phytochelatin accumulation in a newly discovered Cd-hyperaccumulator, Solanum nigrum L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXntFyhtbs%3D&md5=9c0df582c7db2eb3feb55a8650ac3c41CAS |
[19] S. Wei, Q. Zhou, P. V. Koval, Flowering stage characteristics of cadmium hyperaccumulator Solanum nigrum L. and their significance to phytoremediation. Sci. Total Environ. 2006, 369, 441.
| Flowering stage characteristics of cadmium hyperaccumulator Solanum nigrum L. and their significance to phytoremediation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XptVOmtbc%3D&md5=9d200b24f4f46207203c17cb9eadb314CAS | 16859734PubMed |
[20] P. Ji, T. Sun, Y. Song, M. L. Ackland, Y. Liu, Strategies for enhancing the phytoremediation of cadmium-contaminated agricultural soils by Solanum nigrum. Environ. Pollut. 2011, 159, 762.
| Strategies for enhancing the phytoremediation of cadmium-contaminated agricultural soils by Solanum nigrum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnsFWrtg%3D%3D&md5=8b83027a55345e1c320f3ad9e9b81d66CAS | 21185631PubMed |
[21] U. Krämer, I. N. Talke, M. Hanikenne, Transition metal transport. FEBS Lett. 2007, 581, 2263.
| Transition metal transport.Crossref | GoogleScholarGoogle Scholar | 17462635PubMed |
[22] Y. Nevo, N. Nelson, The NRAMP family of metal-ion transporters. Biochim. Biophys. Acta 2006, 1763, 609.
| The NRAMP family of metal-ion transporters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XotFGqurY%3D&md5=302c984ea4e128f3d713b5fc688bd80aCAS | 16908340PubMed |
[23] M. F. Cellier, I. Bergevin, E. Boyer, E. Richer, Polyphyletic origins of bacterial Nramp transporters. Trends Genet. 2001, 17, 365.
| Polyphyletic origins of bacterial Nramp transporters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXksVyntr8%3D&md5=f743dda9f36f241654763d28ccec9d93CAS | 11418195PubMed |
[24] S. Thomine, R. Wang, J. M. Ward, N. M. Crawford, J. I. Schroeder, Cadmium and iron transport by members of a plant metal transporter family in Arabidopsis with homology to Nramp genes. Proc. Natl. Acad. Sci. USA 2000, 97, 4991.
| Cadmium and iron transport by members of a plant metal transporter family in Arabidopsis with homology to Nramp genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXivFKis70%3D&md5=78fe6d6ce67402a77e5ea64ca196e5e6CAS | 10781110PubMed |
[25] R. Cailliatte, A. Schikora, J. F. Briat, S. Mari, C. Curie, High-affinity manganese uptake by the metal transporter NRAMP1 is essential for Arabidopsis growth in low manganese conditions. Plant Cell 2010, 22, 904.
| High-affinity manganese uptake by the metal transporter NRAMP1 is essential for Arabidopsis growth in low manganese conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmsF2ksb8%3D&md5=b18ca28cb59bd451dc793b4af03d4688CAS | 20228245PubMed |
[26] M. Cellier, G. Prive, A. Belouchi, T. Kwan, V. C. Rodrigues, W. P., Gros, Nramp defines a family of membrane protiens. Proc. Natl. Acad. Sci. USA 1995, 92, 10089.
| Nramp defines a family of membrane protiens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXovFamu7c%3D&md5=12175104da08bd8e58774e98ded70332CAS | 7479731PubMed |
[27] M. E. Portnoy, X. F. Liu, V. C. Culotta, Saccharomyces cerevisiae expresses three functionally distinct homologues of the Nramp family of metal transporters. Mol. Cell. Biol. 2000, 20, 7893.
| Saccharomyces cerevisiae expresses three functionally distinct homologues of the Nramp family of metal transporters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnslOjsLw%3D&md5=bfff755dde87734217246e1e6755d9f5CAS | 11027260PubMed |
[28] D. G. Higgins, P. M. Sharp, Clustal: a package for performing multiple sequence alignment on microcomputer. Gene 1988, 73, 237.
| Clustal: a package for performing multiple sequence alignment on microcomputer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXhtV2ns74%3D&md5=22ef795f06ac45827d28eee39b7b9e61CAS | 3243435PubMed |
[29] J. D. Thompson, T. J. Gibson, F. Plewniak, D. G. Higgins, The Clustal X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997, 25, 4876.
| The Clustal X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXntFyntQ%3D%3D&md5=47720da2d83f31f899bf01aaef2b84d5CAS | 9396791PubMed |
[30] J. D. Thompson, D. G. Higgins, T. J. Gibson, W. Clustal, Improving the sensitivity of progressive multiple sequence alignment through sequence weighting position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994, 22, 4673.
| Improving the sensitivity of progressive multiple sequence alignment through sequence weighting position-specific gap penalties and weight matrix choice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXitlSgu74%3D&md5=7508a9d4b92190d4694a91fc62dab763CAS | 7984417PubMed |
[31] K. Tamura, F. U. Battistuzzi, P. Billing-Ross, O. Murillo, A. Filipski, S. Kumar, Estimating divergence times in large molecular phylogenies. Proc. Natl. Acad. Sci. USA 2012, 109, 19333.
| Estimating divergence times in large molecular phylogenies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvValsr7E&md5=0ef47610104446df19a4ed8c5a582aaeCAS | 23129628PubMed |
[32] A. Bernsel, H. Viklund, J. Falk, E. Lindahl, G. von Heijne, A. Elofsson, Prediction of membrane-protein topology from first principles. Proc. Natl. Acad. Sci. USA 2008, 105, 7177.
| Prediction of membrane-protein topology from first principles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmsFCrsb8%3D&md5=cdb6fb47a2a956abea72a3edd29436beCAS | 18477697PubMed |
[33] A. Bernsel, H. Viklund, A. Hennerdal, A. Elofsson, TOPCONS: concensus prediction of membrane protein topology. Nucleic Acids Res. 2009, 37, W465.
| TOPCONS: concensus prediction of membrane protein topology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosFSksL0%3D&md5=838722b2b269b5ae717565930a2901c6CAS | 19429891PubMed |
[34] C. Curie, J. M. Alonso, M. Le Jean, J. R. Ecker, J. F. Briat, Involvement of NRAMP1 from Arabidopsis thaliana in iron transport. Biochem. J. 2000, 347, 749.
| Involvement of NRAMP1 from Arabidopsis thaliana in iron transport.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjsFCjsro%3D&md5=799ed8abeca8dba27c8acf22112c12eaCAS | 10769179PubMed |
[35] M. Yang, W. Zhang, H. Dong, Y. Zhang, K. Lv, D. Wang, X. Lian, OsNRAMP3 is a vascular bundles-specific manganese transporter that is responsible for manganese distribution in rice. PLoS ONE 2013, 8, e83990.
| OsNRAMP3 is a vascular bundles-specific manganese transporter that is responsible for manganese distribution in rice.Crossref | GoogleScholarGoogle Scholar | 24391861PubMed |
[36] D. D. Agranoff, S. Krishna, Metal ion homeostasis and intracellular parasitism. Mol. Microbiol. 1998, 28, 403.
| Metal ion homeostasis and intracellular parasitism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjtF2msb4%3D&md5=4fac3c7a19619de4702590ccfe074c1aCAS | 9632246PubMed |
[37] H. C. Chiang, J. C. Lo, K. C. Yeh, Genes associated with heavy metal tolerance and accumulation in Zn/Cd hyperaccumulator Arabidopsis halleri: a genomic survey with cDNA microarray. Environ. Sci. Technol. 2006, 40, 6792.
| Genes associated with heavy metal tolerance and accumulation in Zn/Cd hyperaccumulator Arabidopsis halleri: a genomic survey with cDNA microarray.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XpvFKisLg%3D&md5=a2117688c5e91a212be44f33caa55c3cCAS | 17144312PubMed |
[38] R. J. Oomen, J. Wu, F. Lelievre, S. Blanchet, P. Richaud, H. Barbier-Brygoo, M. G. Aarts, S. Thomine, Functional characterization of NRAMP and NRAMP4 from the metal hyperaccumulator Thlaspi caerulescens. New Phytol. 2009, 181, 637.
| Functional characterization of NRAMP and NRAMP4 from the metal hyperaccumulator Thlaspi caerulescens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXivFSlsL8%3D&md5=1b6580a32b823b406b074e6433cfc0d2CAS | 19054339PubMed |
[39] A. L. Socha, M. L. Guerinot, Mn-euvering manganese: the role of transporter gene family members in manganese uptake and mobilization in plants. Front. Plant Sci. 2014, 5, 106.
| 24744764PubMed |
[40] M. Tiwari, D. Sharma, S. Dwivedi, M. Singh, R. D. Tripathi, P. K. Trivedi, Expression in Arabidopsis and cellular localization reveal involvement of rice NRAMP, OsNRAMP1, in arsenic transport and tolerance. Plant Cell Environ. 2014, 37, 140.
| Expression in Arabidopsis and cellular localization reveal involvement of rice NRAMP, OsNRAMP1, in arsenic transport and tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVyjurbM&md5=9b64ba4bf58ff4a2ceead62b8da23857CAS | 23700971PubMed |
[41] A. J. M. Baker, Accumulators and excluders – strategies in the response of plants to heavy metals. J. Plant Nutr. 1981, 3, 643.
| Accumulators and excluders – strategies in the response of plants to heavy metals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXhtlemsb8%3D&md5=ca0287ffe269bac85f9311d59087751dCAS |
[42] E. Lombi, F. J. Zhao, S. P. McGrath, S. D. Young, G. A. Sacchi, Physiological evidence for a high-affinity cadmium transporter highly expressed in a Thlaspi caerulescens ecotype. New Phytol. 2001, 149, 53.
| Physiological evidence for a high-affinity cadmium transporter highly expressed in a Thlaspi caerulescens ecotype.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnvF2quw%3D%3D&md5=cb31f9e1ab665ca5746dfa9fbb024266CAS |
[43] W. Zorrig, A. Rouached, Z. Shahzad, C. Abdelly, J. C. Davidian, P. Berthomieu, Identification of three relationships linking cadmium accumulation to cadmium tolerance and zinc and citrate accumulation in lettuce. J. Plant Physiol. 2010, 167, 1239.
| Identification of three relationships linking cadmium accumulation to cadmium tolerance and zinc and citrate accumulation in lettuce.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVaqsLfM&md5=00d98379139e8ab9fe7c9cdfef985754CAS | 20576318PubMed |
