Future Perspectives

This review has focused on the recent progress in understanding the physiological and molecular mechanisms that may be involved in Cd hyperaccumulation and tolerance. In general, the strategies adopted by hyperaccumulating plants aim to absorb and translocate Cd efficiently, and sequester it mostly in the less metabolic active parts, thus to avoid the onset of toxicity. This is achieved by various mechanisms including root proliferation in Cd-rich substrate, influx into cytosol or vacuole by specific or non-specific transporters, and complexation of Cd by certain ligands in cells. Compared to the studies on Zn, however, the mechanisms behind Cd hyperaccumulation are relatively underinvestigated. There are still lots of unclear areas that need to be investigated in the future. Below, and described in Fig. 1, are perspectives regarding the less explored fields associated with the mechanisms and evolution of Cd hyperaccumulation.

A key point of these perspectives is based on the hypothesis that some special hyperaccumulators may have a higher requirement of Cd for optimal growth (Fig. 1). There is substantial evidence that addition of Cd in substrates does enhance the growth of hyperaccumulator species (Table 2). This stimulatory effect has led to two principal questions as to why and how the higher requirement of Cd may be achieved. On the one hand, a better growth of plant in natural metalliferous soils where Cd hyperaccumulators often colonize may have certain ecological advantages, e.g., higher competition and energy storage. This is obtained by enhanced photosynthesis in which Cd may play a role in stimulating the activity of CA and the amount of Rubisco in the Calvin cycle (Liu et al. 2008; Ying et al. 2010). Whether Cd is beneficial for particular plant taxa as shown in marine diatoms (Lane et al. 2005) remains a mystery. Conventionally, this could be determined by studying the phenotypic differences between plants growing in the absence and the presence of Cd (Pilon-Smits et al. 2009). Furthermore, techniques such as chromatography, dichroism spectra, and fluorimetry are required to check if a Cd-containing CA really exists in such Cd hyperaccumulators.

A higher requirement of Cd may also be linked with an efficient elemental defense against herbivores and pathogens. This appears to be the most accepted hypothesis that provides a reasonable explanation for the evolution of metal hyperaccumulation. However, the vast majority of experimental evidence supporting this hypothesis has focused on hyperaccumulators of Ni, Zn, or Se (Boyd 2007) whereas only a few cases for Cd defense have been tested. Further studies such as non-choice and binary choice both in laboratory and in fields are needed to answer two emerging questions. First, what is the minimum concentration of Cd sufficient for defense? Second, can Cd defense be enhanced by the combination of organic defensive compounds, the so-called synergisitc effects hypothesis (Boyd 2007)?

On the other hand, to meet the high requirement of Cd in plant body, hyperaccu-mulators must possess highly efficient mechanisms for uptake and tolerance of Cd. There is strong evidence that certain hyperaccumulators have adopted the root foraging strategy to enhance acquisition of Cd in soil. Root foraging is responsible (even though not entirely) for maintaining high levels of Cd in hyperaccumulators. This trait thus has an important implication toward the improvement of plants to be used in practical phytoextraction, since Cd in soil is often heterogeneously distributed. A big challenge with respect to root foraging is to characterize the molecular and physiological responses involved in the changes in root architecture that are observed in hyperaccumulators, e.g., S. alfredii and T. caerulescens (Liu et al. 2010a; Schwartz et al. 1999, 2003). In terms of the uptake process into roots, numerous evidences have shown that Cd is taken up into root cells by Fe, Ca, and Zn transporters/channels which transport a broad range of substrates. However, a potential Cd-specific uptake system has also been suggested in hyperaccumulator plants (Lombi et al. 2001; Zhao et al. 2002), even though it has not been identified so far. Some other research tools, such as proteomics approaches, could provide a new platform to study the complex biological functions involved in Cd detoxification in hyperaccumulators, such as trafficking, signal transduction, and transport.

Acknowledgments The present research is financially supported by NSFC-Guangdong Joint Foundation of China (No. U0833004), Natural Science Foundation of China (No. 40901151, 31000248), and National High Technology Research and Development Program of China (863 Program) (No. 2007AA06Z305).

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