Chromium speciation modifies root exudation in two genotypes of Silene vulgaris
Introduction
Chromium (Cr) is the second most common metal contaminant in ground water, soil, and sediments due to its wide industrial and agricultural applications. Its toxicity and bioavailability depend strongly on its oxidation state, which ranges from 0 to VI. In the environment, Cr occurs primarily in two valence states, trivalent chromium (Cr III) and hexavalent chromium (Cr VI). The speciation is determined by the biogeochemistry of Cr in soil and water. In general, small concentrations of Cr(VI) can be the result of the natural oxidation of Cr(III), but larger concentrations are usually the result either of pollution with Cr(VI) or of the oxidation of Cr(III) by manganese oxides in ultramafic soils (Dhal et al., 2013). Cr(VI) is water-soluble and hence bioavailable, and the chromate and dichromate ions are fairly strong oxidising agents. Those characteristics make Cr(VI) between 10 and 100 times more toxic than Cr(III) (Deflora et al., 1990), and it is classified as a Group A carcinogen by the EPA (USEPA, 1998).
Phytomanagement could be considered a good alternative for the remediation of Cr-polluted soils because the most mobile forms of Cr in soils can be taken up by plants. This technology uses vegetation, alone or in combination with other technologies, to deliver the most cost-effective means of mitigating any environmental risks associated with the site (Robinson et al., 2009). To develop this technology, a deep knowledge of the relationships between pollutant and plant is required.
The study of plant-Cr has received little attention from researchers due to the lack of Cr functions in plants and of accurate analytical methods for determining the oxidation state of Cr (Shanker et al., 2009). For the last few years, interest in studying Cr as a pollutant has increased because of the development and implementation of phytotechnologies for soil remediation (Dhal et al., 2013, Singh et al., 2013, Choppala et al., 2013). One of the most useful methods for decontaminating Cr-polluted soils is the capacity of certain plants to reduce Cr toxicity by converting highly toxic and readily mobile Cr(VI) into less toxic and less mobile Cr(III) (Chaney et al., 1997). One related process concerns the role of root exudates. In response to Cr(VI) toxicity, plants can release organic compounds that maintain nonessential metals below their toxicity threshold and enhance the accumulation of Cr in the root.
The microbial activity and bacterial communities in soil are greatly influenced by root exudates due to the loss of carbon-containing metabolites from roots into the soil matrix as a result of rhizodeposition (Doornbos et al., 2012). In this way, the border cells and their exudates act as a defence barrier for the roots (Baetz and Martinoia, 2014). In the case of Cr, the organic compounds can form complexes with Cr, thereby making then available for uptake by the root (Hayat et al., 2012); also, microorganisms can use the organic compounds as substrates, resulting in increased microbial activity around the roots, which could affect the remediation effectiveness.
While the rates of exudation vary with species and environmental conditions (Lambers et al., 2009), the composition of root exudates depends on the plant species and cultivar, developmental stage, plant growth substrate and stress factor (Uren, 2000). Under Cr stress, changes in organic acid exudation and rhizosphere pH have been found in different genotypes of rice plants (Zeng et al., 2008). The metal speciation of Cr should affect the exudation rate and composition of the root exudates due to the differences in toxicity exhibited by the Cr species.
Silene vulgaris, the bladder campion, is a perennial dicotyledonous facultative metallophyte widely distributed throughout Europe, North America, Asia and North Africa. The tolerance of this species to a diversity of metals (Ernst and Nelissen, 2000, Jack et al., 2005, Paliouris and Hutchinson, 1991) makes it highly useful in the initial stages of revegetation and soil remediation. Previous studies (Pradas-del-Real et al., 2013) showed that Cr uptake in S. vulgaris was higher in the presence of Cr(VI) than of Cr(III). S. vulgaris presented high diversity at the genotypic level because treatment with hexavalent Cr increased the differences among genotypes. Thus, the use of cuttings from a homogeneous genotype seems to be an adequate method for the study of this species.
The objective of this work was to study whether root exudation in two genotypes of S. vulgaris, which show different tolerances to Cr, could change as a result of exposure to Cr(III) or Cr(VI) to use this species during soil remediation processes.
Section snippets
Plant material and growth condition
Two genotypes of S. vulgaris were chosen from two different populations of Madrid (Spain) according to their different response to Cr(VI) (Pradas-del-Real et al., 2013): (i) genotype SV21 (Rozas de Puerto Real; 200 μM < EC100 Cr(VI) < 1200 μM) and (ii) genotype SV38 (Valdemaqueda; 200 μM < EC100 Cr(VI) < 1000 μM). Clones from each genotype were vegetatively propagated in the field (Alcalá de Henares, Madrid, Spain) in a permanent 10 m × 10 m plot (divided into 1 m2 quadrats). Cuttings of each genotype were
In silico chemical speciation of Cr(III) and Cr(VI) in nutrient solution
In the Cr(VI) treatments (60 and 300 μM), the major Cr chemical species predicted to occur in the nutrient solution were HCrO4− and CrO42−, accounting for 82% and 11%, respectively, of the total Cr(VI). In the Cr(III) treatment, 89.5% of total Cr(III) forms aqueous complexes as CrOH2+, Cr3(OH)45+, Cr2(OH)24+ and Cr(OH)21+. Approximately 6% of the total Cr(III) is predicted to link EDTA as Cr-EDTA. HCrO4− and CrO42− are the most mobile forms of Cr that can be both taken up easily by plants and
Discussion
The question addressed in this study was whether root exudation in S. vulgaris could change as a result of exposure to Cr(III) or Cr(VI) in order to use this species in soil remediation processes. For comparison, we chose two genotypes of S. vulgaris that showed different tolerances to Cr(VI). Based on the results obtained from this study, the answer is positive. In the Cr(VI) treatments, the two genotypes of S. vulgaris released significantly greater quantities of exudates (in terms of mg
Conclusions
The objective of this work was to study whether root exudation in two genotypes of S. vulgaris could change as a result of exposure to Cr(III) or Cr(VI) to explore the use of this species in soil remediation processes. Two genotypes were selected on the basis of their tolerance to Cr. Cr speciation controlled Cr uptake in both genotypes of S. vulgaris because the plants accumulated more Cr in the presence of Cr (VI) than Cr(III). This accumulation caused greater oxidative stress and hence a
Acknowledgements
This work was supported by the Comunidad de Madrid (EIADES S2009/AMB-1478). The authors thank Instituto Madrileño de Investigación y Desarrollo Rural, Agrario y Alimentario for the fellowship support of Ana E. Pradas.
References (44)
- et al.
Effects of high chromium applications on miscanthus during the period of maximum growth
Environ. Exp. Bot.
(2006) - et al.
Root exudates: the hidden part of plant defense
Trends Plant Sci.
(2014) - et al.
Hormesis and plant biology
Environ. Pollut.
(2009) - et al.
Phytoremediation of soil metals
Curr. Opin. Biotechnol.
(1997) - et al.
Chromium contamination and its risk management in complex environmental settings
Adv. Agron.
(2013) - et al.
Genotoxicity of chromium compounds – a review
Mutat. Res.
(1990) - et al.
Chemical and microbial remediation of hexavalent chromium from contaminated soil and mining/metallurgical solid waste: a review
J. Hazard. Mater.
(2013) - et al.
Changes in Salix viminalis L. cv. ‘Cannabina’ morphology and physiology in response to nickel ions – hydroponic investigations
J. Hazard. Mater.
(2012) - et al.
Life-cycle phases of a zinc and cadmium resistant ecotype of Silene vulgaris in risk assessment of polymetallic soils
Environ. Pollut.
(2000) - et al.
Trace element behaviour at the root–soil interface: implications in phytoremediation
Environ. Exp. Bot.
(2009)
Influence of copper on root exudate patterns in some metallophytes and agricultural plants
Ecotox. Environ. Saf.
Chromium interference in iron nutrition and water relations of cabbage
Environ. Exp. Bot.
Do toxic ions induce hormesis in plants?
Plant Sci.
Heavy metal uptake and stress responses of hydroponically cultivated garlic (Allium sativum L.)
Environ. Exp. Bot.
Changes of organic acid exudation and rhizosphere pH in rice plants under chromium stress
Environ. Pollut.
Chromium accumulation by the hyperaccumulator plant Leersia hexandra Swartz
Chemosphere
Metallophytes – a view from the rhizosphere
Plant Soil
Chromium in plants
Beneficial and toxic effects of chromium in plants: solution culture, pot and field studies. Studies in Environmental Science No. 55
Metal hyperaccumulator plants: a review of the ecology and physiology of a biological resource for phytoremediation of metal-pollutes soils
Fungal-associated NO is involved in the regulation of oxidative stress during rehydration in lichen symbiosis
BMC Microbiol.
Impact of root exudates and plant defense signaling on bacterial communities in the rhizosphere. A review
Agron. Sustain. Dev.
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Current address: Geochimie 4D Group, ISTerre, Université Grenoble I, 38041 Grenoble Cedex 9, France.