Chemical speciation of accumulated metals in plants: evidence from X-ray absorption spectroscopy

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Abstract

For centuries, man has been fascinated by the almost magical ability of plants to grow and reproduce on the simplest of materials — sunlight, air, water and minerals. As part of this conjuring act, plants require roots to acquire essential minerals such as iron, copper, nickel, zinc and selenium from the soil. Though these elements are essential, they are also potentially toxic, so plants possess complex biochemistry to control them. For reasons that are not yet clear, plants also have the ability to acquire and detoxify non-essential elements such as arsenic, cadmium, chromium and lead. Using X-ray absorption spectroscopy to probe the oxidation state and chemical speciation of a number of essential and non-essential elements, we have been able to identify certain common themes in the physiology and biochemistry of trace element (hyper)accumulation by plants.

Introduction

It is clear that plants control both the oxidation state and coordination environment of specific elements to maximize either their detoxification, transport, or both. For detoxification of metals and metalloids, plants directly coordinate the element, using the most chemically appropriate ligand, to form stable non-toxic complexes (e.g. with cadmium, zinc and nickel). Alternatively, the element is first chemically reduced to improve its propensity to be strongly coordinated (e.g. arsenic). Chemical reduction can also directly reduce the toxicity of an element (chromium), or be the starting point for the incorporation of non-metals, such as selenium, into organic compounds for detoxification. In this review article we present information on the biochemical interactions of plants with Cd, Zn, Ni, As and Se. This information is based mainly on the utilization of X-ray absorption spectroscopy (XAS).

Section snippets

Cadmium

Cadmium is widely present in soils, and is of concern because many plants accumulate enough to potentially affect human health. Conversely, this ability of plants might be exploited to remediate cadmium contamination of soil and water. Plant cadmium uptake is metabolically mediated, and appears to be competitive with zinc uptake [1]. Much of the Cd remains in the roots, but some is translocated to the shoots. While the mechanism of transport into the roots from the soil water is unknown, though

Zinc and nickel

Zinc and nickel are both essential trace elements, required in only small amounts to perform various coenzyme and regulatory functions. For reasons we still do not fully understand, certain plants accumulate these metals to very high concentrations in their shoots (1–3% of their shoot dry weight) [11]. This extreme habit has even led to a New Caledonian tree [Niemeyera (formerly Sebertia) acuminata] being locally named ‘sève bleue’, because its sap is blue–green due to all the Ni that it

Arsenic

In the early literature, there are numerous reports of arsenic compounds being used to help reduce fever, Black Death, boils and even improve general appearance and ‘well-being’. However, there is no doubt that it is most known for its toxicity, which was recognized even by the ancient Greeks, who preferred to have ‘dispensable’ slaves work their mines. The use of arsenic to poison political opponents and other adversaries must have also been common, as specific laws were passed in the 14th and

Selenium

Selenium is an essential element, but the difference between too little and too much selenium is not very great, and selenium toxicosis is not unusual, at least in herbivores. General Custer might have survived his trip to the Little Bighorn if reinforcements had not been delayed by pack animals apparently suffering from selenium-induced lameness [25]. All plants seem to accumulate some selenium, but hyperaccumulators such as Astragalus bisulcatus are probably the cause of most selenium

Conclusion

It is clear that plants have evolved elaborate systems for the detoxification of trace elements. These systems appear to be tailored to the chemical properties of the elements being detoxified. Of the metals we have investigated, zinc and nickel have the highest preference for oxygen and nitrogen ligands [32]. This is reflected in both zinc and nickel being bound to organic acids and oxygen/nitrogen containing ligands in the plants. On the other hand, cadmium has a higher preference for sulfur

Acknowledgments

This work was supported by the US Department of Energy grant no. DE-FG07-96ER20251 and the US Department of Agriculture grant no. 96-35102-3838 to D.E.S. The Stanford Synchrotron Radiation Laboratory is funded by the US DOE, OBES and OBER; the NIH NCRR, BTP; and the NIGMS.

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