Heavy Metal Hyperaccumulation and Phytoremediation in Plants

Abstract

Hyperaccumulator plants can accumulate extraordinary amount of heavy metals in their aerial organs and they are not negatively affected from heavy metals. Three basic differences distinguish hyperaccumulators from non-hyperaccumulators: an effectively accelerated rate of heavy metal uptake from soil, a faster translocation of heavy metals from roots to shoots and a greater ability of detokxification in leaves. Both hyperaccumulators and non-hyperaccumulators share the common genes and hyperaccumulation ability depends on the different expression and regulation of these genes. In addition, it is an important detail that some haevy metals that are effectively absorbed from soil by hyperaccumulators are essential for plants and animals. In this review, an overview of literature discussing general features of hyperaccumulator plants, phytoremediation types and ability and using these plants for phytomining is presented.

Keywords

• heavy metal
• detoxification
• phytoremediation
• phytomining
• hyperaccumulator

Bitkilerde Ağır Metal Hiperakümülasyonu ve Fitoremediasyon

Abstract

Hiperakümülatör bitkiler çeşitli ağır metalleri toprak üstü organlarında aşırı miktarda biriktiren ancak bundan olumsuz etkilenmeyen bitki türleridir. Hiperakümülatörlerin diğer bitki türlerinden farkı yüksek hızda ağır metal alınımı yapmaları, bu ağır metalleri köklerden gövde ve yapraklara etkili bir şekilde taşımaları ve ağır metaller yapraklarda detoksifiye etmeleridir. Hiperakümülasyon yeteneğinin temelinde, aslında hiperakümülatör olmayan bitkilerde de bulunan bazı genlerin farklı şekilde ekspresyonu ve regüle edilmesi yatmaktadır. Ayrıca hiperakümülatör bitkilerin topraktan etkili bir şekilde absorbe ettiği ağır metallerin bir kısmı canlılar için esansiyeldir. Bu çalışmada hiperakümülatör bitkilerin genel özellikleri, fitoremediasyon kapasitesi ve tipleri ile bu bitkilerin fitomadencilik alanında kullanılabilirliği literatür bilgilerinden faydalanılarak tartışılmıştır.

Keywords

• ağır metal
• detoksifikasyon
• fitoremediasyon
• fitomadencilik
• hiperakümülatör

References

1. La Rocca, N., Andreoli, C., Giacometti, G.M., Rascio, N. ve Moro, I., Responses of the Antarctic microalga Koliella antartica (Trebouxiophyceae, Chlorophyta) to cadmium contamination, Photosynthetica, 47, 471–479, (2009).
2. [2]. Quartacci, M.F., Cosi, E. ve Navari-Izzo, F., Lipids and NADPH-dependent superoxide production in plasma membrane vesicles from roots of wheat grown under coper deficiency or excess, Journal of Experimental Botany, 52, 354, 77-84, (2001).
3. [3]. Watanabe, T. ve Osaki, M., Mechanism of adaptation to high aluminum condition in native plant species growing in acid soils: a review, Communication in Soil Science and Plant Analysis, 33, 1247-1260, (2002).
4. [4]. Rascio, N., Metal accumulation and damage in rice (c.v. Vialone nano) seedlings exposed to cadmium, Environmental and Experimental Botany, 62, 267–278, (2008).
5. [5]. Hall, J.L., Cellular mechanisms for heavy metal detoxification and tolerance, Journal of Experimental Botany, 53, 1–11, (2002).
6. [6]. Sgherri, C., Cosi, E. ve Navari-Izzo, F., Phenols and antioxidative status of Raphanus sativus grown in copper excess, Physiologia Plantarum, 118, 21–28, (2003).
7. [7]. Brooks, R.R., Lee, J., Reeves, R.D. ve Jaffré, T., Detection of nickeliferous rocks by analysis of herbarium specimens of indicator plants, Journal of Geochemical Exploration, 7, 49–57, (1977).
8. [8]. Rascio, N., Metal accumulation by some plants growing on zinc-mine deposits, Oikos, 29, 250–253, (1977).

9. [9]. Chaney, R.L., Malik, M., Li, Y.M., Brown, S.L., Brewer, E.P., Angle, J.S. ve Baker, A.J.M., Phytoremediation of soil metals. Current Opinion in Biotechnology, 8, 279–284, (1997).
10. [10]. Rascio, N., Navari-Izzo, F., Heavy metal hyperaccumulating plants: How and why do they do it? And what makes them so interesting? Plant Science, 180, 169-181, (2011).
11. [11]. Sun, R., Zhou, Q. ve Jin, C., Cadmium accumulation in relation to organic acids in leaves of Solanum nigrum L. as a newly found cadmium hyperaccumulator, Plant and Soil 285, 125–134, (2006).
12. [12]. Macnair, M.R., The hyperaccumulation of metals by plants, Advances in Botanical Research, 40, 63–105, (2003).
13. [13]. Faucon, M.P., Soil influence on Cu and Co uptake and plant size in the cuprophytes Crepidorhopalon perennis and C. tenuis (Scrophulariaceae) in SC Africa, Plant and Soil, 317, 201–212, (2009).
14. [14]. Baker, A.J.M. ve Brooks, R.R., Terrestrial higher plants which hyperaccumulate metallic elements–a review of their distribution, ecology and phytochemistry, Biorecovery, 1, 81–126, (1989).
15. [15]. Verbruggen, N., Hermans, C. ve Schat, H., Molecular mechanisms of metal hyperaccumulation in plants, New Phytologist, 181, 759–776, (2009).
16. [16]. Sagner, S., Hyperaccumulation, complexation and distribution of nickel in Sebestia acuminata, Phytochemistry, 47, 339–347, (1998).
17. [17]. Brooks, R.R., (Ed.), Plants that Hyperaccumulate Heavy Metals, CAB International, Wallingford, UK, 1998, p. 380.
18. [18]. Yang, X.E., Cadmium tolerance and hyperaccumulation in a new Zn hyperaccumulating plant species (Sedum alfredii Hance), Plant and Soil, 259, 181–189, (2004).
19. [19]. Reeves, R.D. ve Baker, A.J.M., Metal-accumulating plants, in: I. Raskin, B.D. Ensley (Eds.), Phytoremediation of Toxic Metals: Using Plants to Clean up the Environment, John Wiley & Sons, 2000, pp. 193–229.
20. [20]. Karimi, N., Ghaderian, S.M., Maroofi, H. ve Schat, H., Analysis of arsenic in soil and vegetation of a contaminated area in Zarshuran, Iran, International Journal of Phytoremediation, 12, 159–173, (2010).
21. [21]. Ma, L.Q., Komar, K.M., Tu, C., Zhang, W. ve Cai, Y., A fern that hyperaccumulates arsenic, Nature, 409, 579, (2001).
22. [22]. Assunçao, A.G.L., Schat, H. ve Aarts, H.G.M., Thlaspi caerulescens, an attractive model species to study heavy metal hyperaccumulation in plants, New Phytologist, 159, 351–360, (2003).
23. [23]. Bert, V., Macnair, M.R., De Laguerie, P., Saumitou-Laprade, P. ve Petit, D., Zinc tolerance and accumulation in metallicolous and nonmetallicolous populations of Arabidopsis halleri (Brassicaceae), New Phytologist, 146, 225–233, (2000).
24. [24]. Bert, V., Genetic basis of Cd tolerance and hyperaccumulation in Arabidopsis halleri, Plant and Soil, 249, 9–18, (2003).
25. [25]. Roosens, N., Verbruggen, N., Meerts, P., Ximenez-Embun, P. ve Smith, J.A.C., Natural variation in cadmium tolerance and its relationship to metal hyperaccumulation for seven populations of Thlaspi caerulescens from Western Europe, Plant Cell and Environment, 26, 1657–1672 (2003).
26. [26]. Assunçao, A.G.L., Elevated expression of metal transporter genes in three accessions of the metal hyperaccumulator Thlaspi caerulescens, Plant Cell and Environment, 24, 217–226, (2001).
27. [27]. Zhao, F.J., Hamon, R.E., Lombi, E., McLaughlin, M.J. ve McGrath, S.P., Characteristics of cadmium uptake in two contrasting ecotypes of the hyperaccumulator Thlaspi caerulescens, Journal of Experimental Botany, 53, 535–543, (2002).
28. [28]. Lombi, E., Zhao, F.J., McGrath, S.P., Young, S.D. ve Sacchi, G.A., Physiological evidence for a high-affinity cadmium transporter highly expressed in a Thlaspi caerulescens ecotype, New Phytologist, 149, 53–60, (2001).
29. [29]. Liu, M.Q., Does cadmium play a physiological role in the hyperaccumulator Thlaspi caerulescens? Chemosphere, 7, 1276–1283, (2008).
30. [30]. Lane, T.W. ve Morel, F.M.M., A biological function for cadmium in marine diatoms, Proceeding of National Academy of Science U.S.A. 97, 4627–4631, (2000).
31. [31]. Meharg, A.A. ve Hartley-Whitaker, J., Arsenic uptake and metabolism in arsenic resistant and non-resistant plant species, New Phytologist, 154, 29–42, (2002).
32. [32]. Caille, N., Zhao, F.J. ve McGrath, S.P., Comparison of root absorption, translocation and tolerance of arsenic in the hyperaccumulator Pteris vittata and the nonhyperaccumulator Pteris tremula, New Phytologist, 165, 755–761, (2005).
33. [33]. Poynton, C.Y., Huang, J.W.W., Blaylock, M.J., Kochian, L.V. ve Ellass, M.P., Mechanisms of arsenic hyperaccumulation in Pteris species: root As influx and translocation, Planta, 219, 1080–1088, (2004).
34. [34]. Gonzaga, M.I., Ma, L.Q., Santos, J.A. ve Matias, M.I., Rhizosphere characteristics of two arsenic hyperaccumulating Pteris ferns, Science and Total Environment, 407, 4711–4716, (2009).
35. [35]. Shibagaki, N., Selenate-resistant mutants of Arabidopsis thaliana identify Sultr1;2, a sulfate transporter required for efficient transport of sulfate into roots, Plant Journal, 29, 475–486, (2002).
36. [36]. Galeas, M.L., Zhang, L.H., Freeman, J.L., Wegner, M. ve Pilon-Smits, E.A.H., Seasonal fluctuations of selenium and sulphur accumulation in selenium hyperaccumulators and related nonaccumulators, New Phytologist, 173, 517–525, (2007).
37. [37]. Lasat, M.M., Pence, N.S., Garvin, D.F., Abbs, S.D. ve Kochian, L.V., Molecular physiology of zinc transport in the Zn hyperaccumulator Thlaspi caerulescens, Journal of Experimental Botany, 51, 71–79, (2000).
38. [38]. Becher, M., Talke, I.N., Krall, L. ve Krämer, U., Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri, Plant Journal, 37, 251–268, (2004).
39. [39]. Hanikenne, M., Evolution of metal hyperaccumulation required cisregulatory changes and triplication of HMA4, Nature, 453, 391–395, (2008).
40. [40]. Colangelo, E.P. ve Guerinot, M.L., Put the metal to the petal: metal uptake and transport throughout plants, Current Opinion in Plant Biology, 9, 322–330, (2006).
41. [41]. Sors, T.G., Ellis, D.R. ve Salt, D.E., Selenium uptake, translocation, assimilation and metabolic fate in plants, Photosynthesis Research, 86, 373–389, (2005).
42. [42]. Callahan, D. L., LC–MS and GC–MS metabolite profiling of nickel (II) complexes in the latex of the nickel hyperaccumulating tree Sebertia acuminata and identification of methylated aldaric acid as a new nickel (II) ligand, Phytochemistry, 69, 240–251, (2008).
43. [43]. Cosio, C., De Santis, L., Frey, B., Diallo, S. Ve Keller, C., Distribution of cadmium in leaves of Thlaspi caerulescens, Journal of Experimental Botany, 56, 565–575, (2005).
44. [44]. Kim, D., The plant CDF family member TgMTP1 from the Ni/Zn hyperaccumulator Thlaspi goesingense acts to enhance efflux of Zn at the plasma membrane when expressed in Saccharomyces cerevisiae, Plant Journal, 39, 237–251, (2004).
45. [45]. Sarret, G., Forms of zinc accumulated in the hyperaccumulator Arabidopsis halleri, Plant Physiology, 130, 1815–1826, (2002).
46. [46]. Sors, T.G., Martin, C.P. ve Salt D.E., Characterization of selenocysteine methyltransferases from Astragalus species with contrasting selenium accumulation capacity, Plant Journal, 59, 110–122, (2009).
47. [47]. Morris, C., Grossi, P.R. ve Call, C.A., Elemental allelopathy: processes, progress, and pitfalls, Plant Ecology, 202, 1–11, (2009).
48. [48]. Freeman, J.L., Quinn, C.F., Marcus, M.A., Fakra, S. ve Pilon-Smits, E.A.H., Selenium tolerant diamondback moth disarms hyperaccumulator plant defense, Current Biology, 16, 2181–2192, (2006).
49. [49]. Tolrà, R.O., Poschenrieder, C., Alonso, R., Barceló, D. Ve Barceló, J., Influence of zinc hyperaccumulation on glucosinolates in Thlaspi caerulescens, New Phytologist, 151, 621–626, (2001).
50. [50]. Chaney, R.I., Plant uptake of inoganic waste constitutes, in: J.F. Parr, P.B. Marsh, J.M. Kla, (eds), land treatment of hazardous wastes, Noyes Data Corp., park Ridge, 1983, pp. 50-76.
51. [51]. Singer, A.C., Bell, T., Heywood, C.A., Smith, JA. C. ve Thompson, I.P., Phytoremediation of mixed-contaminated soil using the hyperaccumulator plant Alyssum lesbiacum: evidence of histidine as a measure of phytoextractable nickel, Environmental Pollution, 147, 74–82, (2007).
52. [52]. Zhao, F.J. ve McGrath, S.P., Biofortification and phytoremediation, Current Opinion in Plant Biology, 12, 373–380, (2009).
53. [53]. Alkorta, I., Hernández-Allica, J., Becerril, J., Amezaga, I., Albizu, I. ve Garbisu, C., Recent findings on the phytoremediation of soils contaminated with environmentally toxic heavy metals and metalloids such as zinc, cadmium, lead, and arsenic, Reviews in Environmental Science and Biotechnology, 3, 71–90, (2004).
54. [54]. Rafati, M., Khorasani, N., Moattar, F., Shirvany, A., Moraghebi, F. ve Hosseinzadeh, S., Phytoremediation potential of Populus alba and Morus alba for cadmium, chromuim and nickel absorption from polluted soil. Int. J. Environ. Res. 5, 961–970, (2011).
55. [55]. Tangahu, B.V., Abdullah, S.R.S., Basri, H., Idris, M., Anuar, N. ve Mukhlisin, M., A review on heavy metals (As, Pb, and Hg) uptake by plants through phytoremediation, International Journal of Chemical Engineering, (2011).
56. [56]. Mukhopadhyay, S. ve Maiti, S.K., Phytoremediation of metal enriched mine waste: a review, Global Journal of Environmental Research, 4, 135–150, (2010).
57. [57]. Mesjasz-Przybylowicz, J., Nakonieczny, M., Migula, P., Augustyniak, M., Tarnawska, M., Reimold, W.U., Koeberl, C., Przybylowicz, W. ve Glowacka, E., Uptake of cadmium, lead, nickel and zinc from soil and water solutions by the nickel hyperaccumulator Berkheya coddii. Acta Biologia Cracovenica Botany, 46, 75–85, (2004).
58. [58]. Singh, S., Phytoremediation: a sustainable alternative for environmental challenges, International Journal of Green and Herbal Chemistry, 1, 133–139, (2012).
59. [59]. Erakhrumen, A.A., Phytoremediation: an environmentally sound technology for pollution prevention, control and remediation in developing countries, Educational Research and Reviews, 2, 151–156, (2007).
60. [60]. Wuana, R.A. ve Okieimen, F.E., Heavy metals in contaminated soils: a review of sources, chemistry, risks and best available strategies for remediation, ISRN Ecology, 2011, 1–20 (2011).
61. [61]. Wu, G., Kang, H., Zhang, X., Shao, H., Chu, L. ve Ruan, C., A critical review on the bio-removal of hazardous heavy metals from contaminated soils: issues, progress, eco-environmental concerns and opportunities, Journal of Hazardous Materials, 174, 1–8, (2010).
62. [62]. Padmavathiamma, P.K. ve Li, L.Y., Phytoremediation technology: hyperaccumulation metals in plants. Water, Air and Soil Pollution, 184, 105-126, (2007).
63. [63]. Vishnoi, S.R. ve Srivastava, P.N., Phytoremediation-green for environmental clean. In: The 12th World Lake Conference, pp. 1016–1021, (2008).
64. [64]. Mukhopadhyay, S. ve Maiti, S.K., Phytoremediation of metal enriched mine waste: a review, Global Journal of Environmental Research, 4, 135–150, (2010).
65. [65]. Yadav, R., Arora, P., Kumar, S. ve Chaudhury, A., Perspectives for genetic engineering of poplars for enhanced phytoremediation abilities, Ecotoxicology, 19, 1574–1588, (2010).
66. [66]. Zorrig, W., Rabhi, M., Ferchichi, S., Smaoui, A. ve Abdelly, C., Phytodesalination: a solution for salt-affected soils in arid and semi-arid regions, Journal of Arid Land Studies, 22, 299–302, (2012).
67. [67]. Manousaki, E. ve Kalogerakis, N., 2011, Halophytes present new opportunities in phytoremediation of heavy metals and saline soils, Industrial and Engineering Chemistry Research, 50, 656–660, (2011).
68. [68]. Ravindran, K.C., Venkatesan, K., Balakrishnan, V., Chellappan, K.P. ve Balasubramanian, T., Restoration of saline land by halophytes for Indian soils. Soil Biology and Biochemistry, 39, 2661–2664, (2007).
69. [69]. Rabhi, M., Ferchichi, S., Jouini, J., Hamrouni, M.H., Koyro, H.-W., Ranieri, A., Abdelly, C. ve Smaoui, A., Phytodesalination of a salt-affected soil with the halophyte Sesuvium portulacastrum L. to arrange in advance the requirements for the successful growth of a glycophytic crop, Bioresouce Technology, 101, 6822–6828, (2010).
70. [70]. Milic, D., Lukovic, J., Ninkov, J., Zeremski-Skoric, T., Zoric, L., Vasin, J. ve Milic, S., Heavy metal content in halophytic plants from inland and maritime saline areas, Central European Journal of Biology, 7, 307–317, (2012).
71. [71]. Shabani, N. ve Sayadi, M.H., Evaluation of heavy metals accumulation by two emergent macrophytes from the polluted soil: an experimental study. Environmentalist, 32, 91–98, (2012).
72. [72]. Li, J.T., Liao, B., Lan, C.Y., Ye, Z.H., Baker, A.J.M. ve Shu, W.S., Cadmium tolerance and accumulation in cultivars of a high-biomass tropical tree (Averrhoa carambola) and its potential for phytoextraction, Journal of Environmental Quality, 39, 1262–1268, (2010).
73. [73]. Tlustoš, P., Száková, J., Hruby, J., Hartman, I., Najmanová, J., Nedelník, J., Pavlíková, D. ve Batysta, M., Removal of As, Cd, Pb, and Zn from contaminated soil by high biomass producing plants, Plant Soil and Environment, 52, 413–423, (2006).
74. [74]. Vamerali, T., Bandiera, M. ve Mosca, G., Field crops for phytoremediation of metal-contaminated land. A review, Environmental Chemical Letters, 8, 1–17, (2010).
75. [75]. Meers, E., Slycken, S.V., Adriaensen, K., Ruttens, A., Vangronsveld, J., Laing, G.D., Witters, N., Thewys, T. ve Tack, F.M.G., The use of bio-energy crops (Zea mays) for ‘phytoremediation’ of heavy metals on moderately contaminated soils: a field experiment, Chemosphere, 78, 35–41, (2010).
76. [76]. Siddiqui, M.H., Kumar, A., Kesari, K.K. ve Arif, J.M., Biomining—a useful approach toward metal extraction, American-Eurasian Journal of Agronomy, 2, 84–88, (2009).