Biological or Physiological Role of Cd

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Cadmium is generally regarded as a non-essential and toxic trace element. However, a Cd-requiring carbonic anhydrase (CA) isolated from the marine diatom T. weissflogii has been characterized as the first Cd-containing enzyme in the biosphere (Lane et al. 2005). Substitution of Zn by Cd to form a Cd-specific CA, particularly under conditions of low Zn, plays a biological role in carbon acquisition and photosynthesis of some marine phytoplanktons (Lane and Morel 2000). It is this important discovery that has generated considerable interest in exploring whether Cd likewise plays a similar physiological or biological function in vascular plants.

Hyperaccumulator species of Cd may be ideal materials to test this hypothesis, because in recent years there is increasing evidence from biological and physiological studies at various levels to support a positive role of Cd in these exceptional species (Table 2, Fig. 1g). At the whole plant level, stimulation of biomass production by addition of Cd in substrates has been observed in most discovered Cd hyperaccumulators (Table 2). The stimulatory effects of Cd on plant growth can vary greatly, depending on the type (ecotype) of species, the growth time, and the substrate tested. For example, Liu et al. (2004) reported by far the greatest increase of approximately 300% of total biomass in Viola baoshanensis when treated hydroponically with 267 p.M Cd, whereas A. halleri showed trivial positive response even at relatively low Cd (5-15 p.M) in solution (Zhao et al. 2006). In S. alfredii, it is noticeable that while less stimulation (17-25%) of shoot dry weight occurred at 12.5-100 p.M Cd in solution (Yang et al. 2004), the total biomass could be increased by about 1.6 or 3.2 times when plants were exposed to 50 or 100 mg kg-1 Cd in soil, respectively (Liu et al. 2010a). This difference may be attributed to the different substrate and experimental duration used. Similarly, Liu et al. (2008) found a significant increase in shoot biomass of T. caerulescens (Ganges) with increasing addition of Cd (5-500 mg kg-1) in soil, whereas the stimulation was not obvious in hydroponic conditions. In general, this phenomenon is similar to hormesis, a toxicological term referring to low-dose stimulation and high-dose inhibition by toxic agents (Calabrese and Baldwin 1998). However, given that the maximum stimulation by Cd in some Cd hyperaccumulators (e.g., 300% in

Table 2 The stimulatory effects of Cd on hyperaccumulator species

Process Plant species Stimulatory dose of Cd Stimulatory phenomenon References and substrate tested associated with Cd

Table 2 The stimulatory effects of Cd on hyperaccumulator species

Process Plant species Stimulatory dose of Cd Stimulatory phenomenon References and substrate tested associated with Cd

Biological character Arabis paniculata

9, 44, 89 |iM in solution

(18^11*)% and (12-39)% increase in shoot and root biomass (DW)

Tang et al. (2009b)

22-89 |iM in solution

(22-27)*% increase in total biomass (FW)

Qiu et al. (2008)

Arabidopsis halleri

5-15 |iM in solution

(5-18)#% increase in root biomass

Zhao et al. (2006)

Picris divaricata

10-25 |iM in solution

(13-27)% and (22-78*)% increase in shoot and root biomass (DW)

Ying et al. (2010)

Potentilla griffithii

44-178 |iM in solution

(25#-56*)% increase in total biomass (DW)

Hu et al. (2009)

Sedum alfredii

12.5-100 |iM in solution

(17-25)% and (2-10)% increase in shoot and root biomass (DW) (NR)

Yang et al. (2004)

50-100 mg kg-1 in soil

(60-220)*% increase in total biomass (DW)

Liu et al. (2010a)

Thlaspi caerulescens (Ganges)

5-500 mg kg-1 in soil

(32-57*)% increase in shoot biomass (DW)

Liu et al. (2008)

1.5 and 3.0 mg kg-1 in

(70-90)#*% increase in shoot

Yanai et al. (2006)

soil

biomass (DW)

Thlaspi caerulescens (St Felix-de-Pallieres)

3 and 30 |iM in solution

37% (14 d) and 75% (31 d) in total biomass (DW) at 3 |iM Cd

Roosens et al. (2003)

Viola baoshanensis

44-267 |iM in solution

(90#-300)% increase in total biomass (DW) (NR)

Liu et al. (2004)

(continued)

(continued)

Table 2 (continued)

Process

Plant species

Stimulatory dose of Cd and substrate tested

Stimulatory phenomenon associated with Cd

References

Morphological

Sedum alfredii

50-100 mg kg"1 in soil

Root proliferation (over 90%)

Liu et al. (2010a)

character

in Cd-rich patches

Thlaspi caerulescens (Clough)

0/500 mg kg"1 CdS in soil

Root proliferation in Cd-rich patches

Whiting et al. (2000)

Thlaspi caerulescens (Prayon and Viviez)

&

Root proliferation in hot spots of Cd

Schwartz et al. (2003)

Physiological

Arabis paniculata

9-178 |iM in solution

Increase in chlorophyll

Tang et al. (2009b)

character

contents

22-89 |iM in solution

Alleviation of ROS (MDA, 02"\ H2O2) stress in roots

Qiu et al. (2008)

Picris divaricata

5-50 |iM in solution

Increase in CA activity and Rubisco content

Ying et al. (2010)

Sedum alfredii

200-1,000 |iM in solution

Increase in chlorophyll contents

Zhou and Qiu (2005)

Thlaspi caerulescens (Ganges)

0-50 |iM in solution

Increase in CA activity

Liu et al. (2008)

5-50 |iM in solution

Evidence for a high-affinity Cd uptake system

Lombi et al. (2001)

An asterisk denotes that stimulatory effect is significant compared with the control A symbol # denotes that the data are estimated from the figure of the corresponding reference A symbol & denotes that Cd levels are not given using inclusions of Cd shots into uncontaminated soil NR means that significance of stimulatory effect is not reported in reference

An asterisk denotes that stimulatory effect is significant compared with the control A symbol # denotes that the data are estimated from the figure of the corresponding reference A symbol & denotes that Cd levels are not given using inclusions of Cd shots into uncontaminated soil NR means that significance of stimulatory effect is not reported in reference

V. baoshanensis; 220% in S. alfredii; and 90% in Ganges of T. caerulescens, Table 2) is much higher than the typical range of 30-60% stimulation that is documented in many hormetic studies (Calabrese and Baldwin 1998), this might not simply be a general case of hormesis - it is possible that Cd has acquired a biological role in some exceptional hyperaccumulator species (Roosens et al. 2003).

From the morphological perspective, a positive response to Cd-enriched hot spots by roots of T. caerulescens has been reported (Schwartz et al. 1999, 2003; Whiting et al. 2000). This trait can be much more significant in S. alfredii, in which approximately 90% of root biomass is allocated to the Cd-enriched patches, suggesting that a root foraging strategy for Cd similar to that mostly occurring in nutrient acquisition in heterogeneous soils has evolved and plays a role in Cd hyperaccumulation (Liu et al. 2010a). The underlying mechanisms of such non-directional development of root architecture by Cd heterogeneity are yet to be shown, but may be linked with an auxin-regulated signal sensing process, like that observed in root branching by nitrate (Zhang et al. 1999).

Cadmium may also improve physiological processes in hyperaccumulator species (Table 2). Stimulatory effects in leaf chlorophyll synthesis have been reported in A. paniculata (Tang et al. 2009b) and S. alfredii (Zhou and Qiu 2005). The increase in chlorophyll content in the latter might be a result of Cd-induced increase in Fe uptake (Zhou and Qiu 2005). Meanwhile, the amounts of malondialdehyde (MDA), O2-1, and H2O2 in roots of A. paniculata decreased significantly at 22-89 p.M Cd levels, suggesting that moderate addition of Cd may alleviate the oxidant stress caused by Cd-induced ROS (Qiu et al. 2008). With respect to photosynthesis, Liu et al. (2008) and Ying et al. (2010) found that the CAs activity in T. caerulescens and P. divaricata correlated positively with the shoot Cd concentration, demonstrating that Cd may play a physiological role in Cd hyperaccumulation (Fig. 1f). Further study is needed to elucidate the biological function of Cd in hyperaccumulators through enzymological and molecular methods.

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