Contrasting effects of Cr(III) and Cr(VI) on lettuce grown in hydroponics and soil: Chromium and manganese speciation
Graphical abstract
Introduction
Chromium (Cr) is considered a toxic element, and the toxicity of Cr is determined by its oxidation state. Hexavalent chromium [Cr(VI)] is more toxic and mobile, while trivalent chromium [Cr(III)] is known to be less toxic or non-toxic (Shanker et al., 2005; Jin et al., 2016). Hexavalent Cr is taken up by roots through the phosphate and sulfate pathway and easily transported to other parts of the plant, whereas Cr(III) is transported through a passive pathway (Cornelis et al., 2005; Smith et al., 1989). Phytotoxic effect of Cr(VI) includes decreased germination rate, limited root growth, and subsequent decreased nutrients and water transport in plants. In addition, Cr(VI) affects physiological processes including photosynthesis and enzyme activity, and causes genotoxicity (Oliveira, 2012). Vignati et al. (2010) reported, however, that Cr(III) could be more toxic to green algae when soluble Cr(III) concentration was considered. Elsewhere, it was reported that Cr(III) inhibits seed germination and hypocotyl elongation and reduced chlorophyll content in celery seedlings (Scoccianti et al., 2006).
Chromium can be oxidized or reduced under various soil conditions (James et al., 1997). The oxidation and reduction reactions of Cr can occur spontaneously and simultaneously (Shahid et al., 2017). Several soil components were related to the Cr speciation where soil pH, organic matter contents, and calcium carbonate were reported as the most important factors controlling Cr species (Köleli, 2004). Trivalent Cr is known to be oxidized in the presence of oxidized Mn, where Mn acts as an electron acceptor (Bartlett and James, 1979; Fendorf and Zasoski, 1992). In soils, Mn originates from minerals such as serpentine, pyroxene, and amphibole, which was correlated with Cr (Kazakis et al., 2015). The Cr oxidation was also related to soil water content because of different stability of Mn(III, IV) oxide under different soil water content (Trebien et al., 2011). The oxidation of Cr(III) to Cr(VI) involved the formation of Cr(III) complex on Mn oxide surfaces, electron transfer between Cr(III) and Mn (III or IV), and release of Mn(II) and Cr(VI) in soil solution (Trebien et al., 2011). However, limited oxidation of Cr(III) by Mn(IV) oxide was observed although the reason was not found and was not related to the surface precipitation of Cr(OH)3 (Landrot et al., 2012). Especially, oxidation of Cr was reported to occur in soils with high Mn(IV) oxide and low organic matter contents (Kožuh et al., 2000). Hexavalent Cr can be reduced by organic matter, Fe(II), and sulfide (Fendorf and Zasoski, 1992). Compost and peat reduced water-soluble and exchangeable total Cr and Cr(VI) in soil, and Cr accumulation and phytotoxic effect in plants also decreased (Rendina et al., 2011). Soil is a complex medium composed of organic matter and various elements that affect Cr redox reaction. Therefore, the toxicity of Cr(III) and Cr(VI) spiked in solution and soil might be different, and information on Cr speciation is important for risk assessment and remediation of water and soil (Shahid et al., 2017).
Although Cr speciation and toxicity can be different between Cr(III) or Cr(IV) treated hydroponics and soil, comparative studies of plant growth and Cr speciation in both Cr(III) and Cr(VI) spiked water and soils are limited. In addition, oxidation state and release of Mn was not studied in relation to Cr oxidation and reduction despite of their close interdependence. Therefore, the objectives of this study were to evaluate Cr speciation in lettuce and to investigate lettuce growth, and Cr and Mn speciation in Cr(III) and Cr(VI) spiked soils. In this study, X-ray absorption spectroscopy (XAS) was used to determine Cr speciation in lettuce and soils. The different toxic effects of spiked Cr(III) and Cr(VI) in hydroponics and soil were compared, and possible reasons for the differences were suggested.
Section snippets
Lettuce growth and Cr treatment in hydroponics
Lettuce (Lactuca sativa) seeds were sown and germinated in a germination sponge (2.5 × 2.5 × 3 cm) containing 1/5 strength Hoagland solution in a seed tray before exposure to Cr. The 1/5 strength Hoagland solution contained 1 mM KNO3, 0.5 mM Ca(NO3)2·4H2O, 0.4 mM MgSO4·7H2O, 0.2 mM NH4NO3, 0.036 mM Fe(NO3)3·9H2O, 0.1 mM KH2PO4, 9.26 × 10−3 mM H3BO3, 2.4 × 10−3 mM MnCl2·4H2O, 1.53 × 10−4 mM ZnSO4·7H2O, 4.09 × 10−5 mM CuSO4·5H2O, and 9.92 × 10−3 mM Na2MoO4·2H2O. After germination, the seedlings
Lettuce growth in hydroponics and soils containing Cr(III) and Cr(VI)
Lettuce exposed to Cr(III) and Cr(VI) in hydroponics showed reduced leaf and root growth compared with the control (data not shown). In particular, lettuce grown in Cr(VI) treated hydroponics developed overall chlorotic leaves and interveinal chlorosis in young leaves, and the old leaves of lettuce grown in Cr(III) treated hydroponics turned green-yellow. Chromium is known to be toxic to plants and its toxicity depends on the oxidation states of Cr. Generally, Cr(VI) is more toxic and mobile
Conclusions
The Cr valence state was Cr(III) in lettuce leaves and roots regardless of treated Cr species both in hydroponics and soil. Lettuce transformed Cr(VI) to Cr(III) in plant tissue in Cr(VI) treated nutrient solution, and soil organic matter transformed Cr(VI) to Cr(III) in Cr(VI) spiked soil. The different translocation rate of Cr from lettuce roots to shoots for Cr(III) and Cr(VI) in hydroponics indicates a different uptake mechanism of these by lettuce roots. The Cr speciation was similar to
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
This study was financially supported by the National Research Foundation of Korea (NRF) grant, funded by the Korea government (MIST) (No. 2017R1C1B5075522). Experiments at PAL were supported in part by MSIP and Pohang University of Science and Technology (POSTECH).
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