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Remediation of Heavy Metals Contaminated Saline Soils: A Halophyte Choice? Hong-Ling Wang,† Chang-Yan Tian,‡ Li Jiang,‡ and Lei Wang*,‡ †

Key Laboratory of Biogeography and Bioresource in Arid Land, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi 830011, China ‡ State Key Laboratory of Desert and Oasis Ecology, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi 830011, China cost, environment friendly and effective method for decontamination of heavy metals polluted soils. Exploring and selecting stabilizers and accumulators or even hyperaccumulators for heavy metals is a key step for successful phytoremediation. When facing with the combined pollution caused by salt and heavy metals, it is impossible to remediate heavy metals contaminated saline soils by using glycophyte accumulators because glycophytes would die in saline environments. However, halophytes, which are about 1% of the world’s flora, are unique plants that can grow in saline soils. Halophytes potentially have high resistance to heavy metals that is strongly linked to characteristics for salt resistance. First of all, synthesis of osmoprotectants helps halophytes to resist heavy metal stresses. In order to maintain suitable water potential and to protect cellular structure in saline environments, halophytes synthesize osmoprotectants. Since heavy metals also induce secondary water stress and oxidative damage to cellular structure, the capacity of halophytes to synthesize these osmoprotectants may be involved in dealing with heavy metals. Also, antioxidants synthesis of halophytes improves resistance against oxidative stress caused by heavy metals. Halophytes tend to have higher levels of activity for superoxide ith the increasing urbanization, industrial development dismutase (SOD), catalase (CAT) and peroxidase, and have and extensive application of agricultural chemical lower levels of damage to their lipid membrane from reactive substances, soil contamination with heavy metals is becoming oxygen species under heavy metal stresses. For example, more and more serious in the world, including saline soils. halophyte Salicornia brachiata can up-regulate the activity of Many salt marshes and large tracts of oasis farmland in arid and CAT and SOD in response to heavy metals such as Cd, Ni, and semiarid regions are affected by salinity and polluted by heavy As.4 Generally, Antioxidant systems of halophytes are more metals.1,2 So far, several approaches have been applied to efficient than those in glycophytes at scavenging free radicals remediate heavy metals contaminated saline soils. However, the resulting from heavy metal stresses. Moreover, some halophytes remediation effects were limited because of the complexity of utilize salt excretion mechanism to excrete heavy metal ions. In combined pollution, immature technology, and the high cost. some cases glandular tissues of halophytes not only excrete Na+ and Cl−, but also remove heavy metal ions from photosynthetiPotentially halophytes are resistant not only to salt but also to cally active tissues onto the leaf surface. In short, halophytes heavy metals because plant resistance to different stresses partly have high resistance to heavy metals due to their salt resistance rely on common physiochemical mechanisms.3 Furthermore, mechanisms. many halophytes can accumulate or excrete heavy metals. Halophytes have several additional advantages for heavy Therefore, halophytes are suggested as the optimal candidates metals phytoremediation in saline soils. First, for some for phytostabilization or phytoextraction of heavy metals halophytes, salt is a key promoter in the translocation of contaminated saline soils. Here, we propose that selecting heavy metals from roots to shoots. For instance, for the whole target halophytes that can accumulate moderate concentration plant of halophyte Tamarix smyrnensis, total Cd removal from of heavy metals and produce high biomass yields may be a soil increased from 9.4 μg in the absence of salt to 19.7 μg at convenient and efficient means for this phytoremediation purpose, based on the fact that heavy metal hyperaccumulating halophytes are difficult to obtain and usually have low biomass. Received: November 13, 2013 Halophytes are probably the only candidate for phytorRevised: December 5, 2013 emediation of heavy metal polluted saline soils. PhytoremediaAccepted: December 16, 2013 Published: December 23, 2013 tion, which is considered as a green alternative solution, is a low

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© 2013 American Chemical Society

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0.5% NaCl and to 38.3 μg at 3% NaCl.5 Second, salinity can improve heavy metal bioavailability in soils, especially for mobile heavy metals. Third, many halophytes can also accumulate large amounts of salt while extracting heavy metals from saline soils. What kind of halophytes should we choose for the purpose of phytoremediation? Selecting heavy metal hyperaccumulating halophytes may not be the most efficient method because they are difficult to obtain. More than 400 plant species have been identified as heavy metal hyperaccumulators, but as far as we know, few of them are halophytes. What make us even more frustrated is that most hyperaccumulators do not have very high biomass. So we can not directly use these plants to effectively remediate heavy metals in saline soils, and need to reselect target plants from halophytes. It might be a viable and effective alternative to select halophytes that can accumulate moderate concentration of heavy metals and produce high biomass yields. Although heavy metal concentrations in many halophytes are at low to moderate levels, high biomass suggests that the heavy metal extraction efficiency of these halophytes is higher than that of hyperaccumulators. There are two possible ways to select halophytes for the purpose of phytoremediation. For one thing, halophytes can be selected for phytostabilization. Some halophytes have extensive root system and accumulate heavy metals in their roots, but not accumulate heavy metals into their aerial parts. This kind of halophytes provides opportunity for phytostabilization application. On the other hand, halophytes can be chosen for phytoextraction. Halophytes that mainly accumulate metals into aerial parts are suitable for this purpose. Basically, we need to pay special attention to combined effects of salinity and heavy metals in plants and soils. In short, developing halophyte remediation technologies may help solve the heavy metal problems occurred in saline soils or even nonsaline soils.



AUTHOR INFORMATION

Corresponding Author

*Phone: +86-991-7823189; fax: +86-991-7885320; e-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work is supported by the West Light Foundation of the Chinese Academy of Sciences (XBBS201101). REFERENCES

(1) Duarte, B.; Caetano, M.; Almeida, P. R.; Vale, C.; Caçador, I. Accumulation and biological cycling of heavy metal in four salt marsh species, from Tagus estuary (Portugal). Environ. Pollut. 2010, 158 (5), 1661−1668. (2) Wang, X.-J. Distribution of several soil heavy metals and pollution evaluation in Changji typical region, Xinjiang. M.S. Dissertation, Xinjiang Agricultural University, Urumqi, CN, 2011. (3) Manousaki, E.; Kalogerakis, N. Halophytes-An emerging trend in phytoremediation. Int. J. Phytorem. 2011, 13 (10), 959−969. (4) Sharma, A.; Gontia, I.; Agarwal, P. K.; Jha, B. Accumulation of heavy metals and its biochemical responses in Salicornia brachiata, an extreme halophyte. Mar. Biol. Res. 2010, 6 (5), 511−518. (5) Manousaki, E.; Kadukova, J.; Papadantonakis, N.; Kalogerakis, N. Phytoextraction and phytoexcretion of Cd by the leaves of Tamarix smyrnensis growing on contaminated non-saine and saine soils. Environ. Res. 2008, 106 (3), 326−332.

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Remediation of heavy metals contaminated saline soils: a halophyte choice?

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