Heavy Metal Pollution in China

Review Articles

Effects of Heavy Metals on Plants and Resistance Mechanisms

A State-of-the-Art Report with Special Reference to Literature Published in Chinese Journals

ShuipingCheng
State Key Lab of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, The Chinese Academy of Sciences, Wuhan, 430072, P.R. China, and Institute of Botany, University of Cologne, Gyrhofstrasse 15, D-50931 Koeln, Germany (shpcheng@public.wh.hb.cn)
Introduction

DOh http://dx.doi.or~10.1065/espr2002.11.141.2 Abstract

Goal, Scope and Background. As one of the consequences of heavy metal pollution in soil, water and air, plants are contaminated by heavy metals in some parts of China. To understand the effects of heavy metals upon plants and the resistance mechanisms, would make it possible to use plants for cleaning and remediating heavy metal-polluted sites. Methods. The research results on the effects of heavy metals on plants and resistant mechanisms are compiled from Chinese publications from scientific journals and university journals, mostly published during the last decade. Results and Discussion. Effects of heavy metals on plants result in growth inhibition, structure damage, a decline of physiological and biochemical activities as well as of the function of plants. The effects and bioavailability of heavy metals depend on many factors, such as environmental conditions, pH, speciesof element, organic substances of the media and fertilization, plant species. But, there are also studies on plant resistance mechanisms to protect plants against the toxic effects of heavy metals such as combining heavy metals by proteins and expressing of detoxifying enzyme and nucleic acid, these mechanisms are integrated to protect the plants against injury by heavy metals. Conclusions. There are two aspects on the interaction of plants and heavy metals. On one hand, heavy metals show negative effects on plants. On the other hand, plants have their own resistance mechanisms against toxic effects and for detoxifying heavy metal pollution.
Recommendations and Outlook. To study the effects of heavy metals on plants and mechanisms of resistance, one must select crop cuhivars and/or plants for removing heavy metals from soil and water. More highly resistant plants can be selected especially for a remediation of the pollution site. The molecular mechanisms of resistance of plants to heavy metals should be studied further to develop the actual resistance of these plants to heavy metals. Understanding the bioavailability of heavy metals is advantageous for plant cultivation and phytoremediation. Decrease in the bioavailability to farmlands would reduce the accumulation of heavy metals in food. Alternatively,one could increase the bioavailability of plants to extract more heavy metals.
Keywords: Accumulation; bioavailability; cell division; enzyme; growth; metallothionein; phytochelator; phytoremediation; pollution; structure
II[I

As one of the consequences of heavy metal pollution in soil, water and air in some cases in China (Guo 1994, Liao 1993, Suet al. 1994, Wu et al. 1989), plants were also seen to be polluted by heavy metals ( D u e t al. 1999, Wu et al. 1998, Yin et al. 1999, Zhang et al. 1996), which consequently threatens the health of animals and human beings via the foodchain (Wang et al. 2001). it is urgently necessary to clean and remediate heavy metals from areas, where crops, vegetables, fruits and pasturages have been grown, in order to protect the health of animals and human beings. Plants play an important role in solar energy transport to bio-energy and can clean the environment in an environmentally friendly manner, they would also play an important role in heavy metal remediation. To understand the effects of heavy metals on plants and resistance mechanisms would be helpful for using plants to clean and remediate heavy metal pollution. In China, there are many reports on the interaction of heavy metals and plants (Zhao and Bi 1999, Zhang and Huang 2000). In this review, the author compiles the research results of the interaction of heavy metals and plant which have mostly been published in Chinese within the last decade, in order to make this information internationally accessible, but also to provide basic theories to develop phytoremediation techniques.
1 1.1 Effects of Heavy Metals on Plants Effects of heavy metals on the growth of plants

Heavy metals such as Cd and Pb are non-essential elements for plants. If plentiful amounts are accumulated in the plants, heavy metals will adversely affect the absorption and transport of essential elements, disturb the metabolism, and have an impact on growth and reproduction (Xu and Shi 2000). The germinating ratio and growth rate of barley declined, for instance when polluted by Cd, and the decline was related to the dosage and duration. The germinating ratio was lower than 45 % and the growth of roots were stagnant under 10-2 mol/L Cd treatment (Zhang 1997). The seedlings of bean became brown and died under Cd stress (Mo and Li 1992). The roots were one of the target organs of Cd pollution, so that the root growth of crops such as wheat (Xia 1988, H0ng et al. 1991), maize, pumpkin (Liu and Cui 1991), cucumber (Chen 1990), and garlic (Allium sativum L ) (Liu et al. 2000) were inhibited.

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Seedlings represent a more easily damaged stage of the life cycle. In crops such as rice and cotton (Qin et al. 2000), and vegetables such as spinach (Spinacia oleracea Linn.) (Song et al. 1996), Brassica chinensis L. (Zhou et al. 1997) and Brasenia schreberi L. (Yang et al. 2001), seedlings were easily injured and inhibited by the heavy metal pollution in a hydroponical exposure. The growth of vegetables such as cabbage, carrots, broccoli and cucumbers were inhibited under exposure to 10 mg/L Cd solution (Liu et al. 1995). Yang et al. (1999a) studied the effects of Cr 6+on Hydrochairs dubia(B.l) Backer and showed that Cr prevented it from absorbing water. The degree of damage was positively relative to the cultural concentration and time. At a high concentration of Cr 6+ (16-32 mg/kg), the edge of the leaves began to dry and the root tips rotted in a short period of time. The effects of heavy metals on plants are different in different growth stages of plants. In the early stage, Cd inhibits the photosynthesis and growth of rice, then inhibits the reproductive organs' differentiation, and finally distributes the nutrients transport and mobilization (Wang 1996), but a low concentration of Hg (10 -s mol/L) stimulated the growth of wheat seedlings. The reason for this may be that low concentrations of Hg increased the activities of amylase, proteinase and lipase, sped up the decomposition of endosperm and the respiration rate, so that the germination was more rapid (Ma and Hong 1998). Root vitality is reduced under heavy metal stress. Shu et al. (1997) measured the root vitality of Stylosanthes guianensis in mine tailings, it was reduced by heavy metals (Pb, Zn, Cu and Cd), and the absorption of inorganic nutrients was prevented and led to evident chlorosis, which significantly affected the growth.
1.2 1.2.1 Effects of heavy metals on the cell division of plants Effects on the cell division cycle and the cell division exponent

by low concentration heavy metals (Pb 1.0 ppm and Cd 0.01 ppm), the cell division exponent raised from 16% to 20%, while increasing the concentrations of heavy metals, the cell division exponent declined and revealed a negative relationship to the dosage of heavy metals (Duan and Wang 1995). But it did not show such results following different concentrations of Hg treatment. Hg inhibited the cell division of beans, garlic and onions (Mo and Li 1992, Zhao and Mo 1997). The low and high dosage of heavy metals revealed opposite effects on the same physiological activity of plants, which means a stimulation reaction of plants to low heavy metal stress. In the procedure, physiological and biochemical activities of plants are sped up, producing plentiful amounts of metabolized products such as glutathione (GSH), oxalic acid, histidine, citrate and metal-binding proteins to combine heavy metals and to detoxify (Zhang et al. 1999). The high dosage of heavy metals, on the other hand, results in a speedier metabolism and increases the entrance of heavy metals into cells. If the metabolism is inhibited, toxicity to the plants is revealed (Zhao and Bi 1999).
1.2.2 Effects on the form of chromosome

Heavy metals affect the cell division of plants, and the effects are different and depend on the concentration. Mo and Li (1992) studied effects of Cd on the cell division of root tips in beans. Duan and Wang (1995) treated the beans by using Cd, Pb and Zn. These results showed that the cell division was extended under a low concentration of 0.01, 1.0 and 10 ppm of Cd, Pb and Zn, respectively, while cell division was shortened but the cell cycle was extended by increasing the dose. Zhang (1997) investigated the effects of Cd, Hg and Pb on the cell division of barley (Hordeum vulgate Linn.) and also showed the trend of cell cycle extension under the 0.01 mol/L concentration treatment. And Cd, Hg and Pb also combined with nuclear acid and damaged the structure of the nucleolus after 24 hrs of treatment with a 0.005-0.0005 mol/L dosage, inhibited the DNase and RNase activities (Duan and Wang 1992), thus resulting in the interruptive synthesis of DNA (Yang and He 1995a) to affect cell division. Treated by heavy metals, the cell division exponent is changed, and relates to the elements and treatment manner. Treated

The genotoxicity of heavy metals in plants influences the synthesis, and the duplication of DNA and chromosomes both directly or indirectly, as well as inducing chromosomal aberration. The effects relate positively to heavy metal dosage. Zhang (1997) treated the barley by Cd and showed that Cd combined with nuclear acid and damaged the structure of the nucleolus, as well as causing chromosome fragmentation, aberration, conglutination and liquefaction. Exposed to Cd, Pb, Hg, the chromosomes of beans, garlic and onions were injured and revealed polyploid, C-karyokinesis, chromosomal bridges, chromosomal rings, and chromosome fragmentation, chromosome fusion, micro-nuclei and nuclear decomposition (Mo and Li 1992, Liu et al. 1992, Duan and Wang 1995, Zhao and Mo 1997). The high concentration of heavy metals in medium, in which plants could not grow normally, affected the SCE (sister chromatid exchange) frequency in root tip cells of Hordeum vulgare. Cr203 or CdC12 could be detected by SeE tests even if there is a lower dose level (Yi and Zhang 1997).
1.3 1.3.1 Effects of heavy metals on structures of plants Effects of heavy metals on the ultrastructure of cells

The grana cascade of chloroplast mitochondria decrease, disappear or swell, and polypeptide compositions of the thylakoid membrane are degraded under heavy metal stress. Peng and Wang (1991) studied the effects of Cd on the cell uhrastructure of maize and showed that the grana cascade of chloroplast mitochondria decreased and/or disappeared under low concentrations of Cd stress. Otherwise, the chloroplast cascade became more extensive and the membranes began to decompose, the mitochondria also became tumorous and decomposed under high concentrations of Cd stress. The damage to the chloroplasts was related to the attach-

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Pb, Cd and Zn influence the conformation of wheat DNA and change DNA UV absorption peak value. Pb has the greatest effect on the DNA conformation, the hypochromicity and the separation of DNA. The effect of Cd is relatively small and may result in a slight hypochromicity. Zn of low concentration (100 mg/L) leads to hypochromicity as well (Meng et al. 1998a).
1.3.2 Effects of heavy metals on cell membrane

ment of Cd to the thylakoid and combined with the protein in the membrane to destroy the enzymatic system of the chloroplasts and to block the synthesis of chlorophyll. Hydrocharis dubia L. demonstrated that the chromatin condensed, and the thylakoids of chloroplast and lumen of mitochondria swelled in the early stages when the leaves suffered poisoning due to Hg (Hao et al. 2001). Also, the polypeptide compositions of the thylakoid membrane of B. schreberi were degraded under the stress of Hg and Cd (Chen et al. 1999). The changes in the mitochondria resulted from the penetration of K and H20 from the lumen to the outside and the disturbance of Cd on the activities of ATE Yang (1991) also reported the effects of heavy metals on the structure and function of photosynthetic membranes of higher plants and showed that the sub-microstructure of chloroplast were changed. The grana also decomposed and some plasmids were formed. In intact tobacco (Nicotiana tabacure), the photosynthetic membranes were damaged by Cd treatment, which might be the main reason for the decreasing of photosynthetic intensity (Jiang 1995). Palisade and spongy mesophyll, and the disintegration of cells, were destroyed under Cd and Hg stress (Li et al. 1998, Li and Shi 1999, Li et al. 1999a). Under the stress of Hg, in mature leaves of Brasenia schreberi L., it was observed that palisade and spongy mesophyll were destroyed and that there was a disintegration of cells when mixtures flew into cell crevices; the basic microstructure of the petiole did not change, but the starch grains almost disappeared. In young leaves, although the microstructure did not change as well, the number of starch grains decreased very much, especially starch grains in the cell layer which was under the upper epidermis (Li et al. 1998). Li et al. (1999a) treated floating leaves of Trapa bicornis Osbeck with Cd at a concentration of 50 and 100 pmol/L. The cells were seen to be out of shape and broken; the tissues came loose and deformed, including the destruction of the palisade and spongy mesophyll. In the cells of the leaves, nuclear substance disappeared, but the nuclear membrane remained intact. The number of chloroplast grana decreased, the layers of grana disintegrated and the chloroplast envelope became disrupted. The ultrastructure of nuclei and chloroplasts in stomata of T. bicornis treated by Cd and Hg (10-50 l~mol/LCd or Hg solution) was also studied (Li and Shi 1999) and the degree of destruction was seen to have increased as the concentration of heavy metal solution rose. Under Cd stress, electron dense globules were unusually deposited in the vacuoles in the root tip cells of garlic (A. sativum) (Liu et al. 2000). These globules, whose electron density was greater outside than inside, were big or small, and distributed near the vacuoles in the cytoplasm. Nucleoplasm in most of the nuclei was highly condensed, and other effects like a formation of plasmolysis, disintegration of cell organelles was revealed as well. The results from X-ray microanalysis showed that there were no Cd ions in these globules and indicated that the epidermal cells of the root tip treated with higher concentration of Cd (10-2 mol/L) appeared to be more hardened; the cell walls obviously increased in thickness and many mucilage exudates were deposited in the cell walls.

The enzyme system is the interface and barrage between the cell and environment for substance and information exchange. The stabilization of this enzyme system is the basis for the physiological functions in the cell. Cd damages the enzyme system and increases the penetration of cell membrane (Hong et al. 1991, Li et al. 1992), and there is a significant relationship between the penetration of cells and the concentration of Cd (Sun and Wang 1985). The absorption polypeptide compositions of the thylakoid membrane of the macrophyte Brasenia schreberi were degraded under Hg and Cd stress. It was also shown that the toxic effects of Hg on B. schreberi winter buds were more significant than those seen for Cd (Chen et al. 1999). Under Cd treatment, the accumulation of 02, H202 and malondialdehyde (MDA) in wheat (Triticum aestivum L.) leaves were significantly enhanced, the content of SH group dropped, and the electrolyte leakage out of the leaf cells was much higher, it indicated lipid peroxidation of cellular membrane was stimulated by endogenously active oxygen radicals (Luo 1999).
1.4 Effects of heavy metals on physiological and biochemical characteristics of plants

1.4.1 Content of chlorophyll and the photosynthesis system

Effects of heavy metals on the content of chlorophyll and photosynthesis yield depend on the concentration of heavy metals. Exposed to Cr 6+, the content of chlorophyll of H. dubia leaves rose in the solution of 4 and 8 mg/kg in the first few days, although it was reduced in 16 and 32 mg/kg treatments (Yang et al. 1999a). The same results were observed for B. schreberi, where the content of chlorophyll decreased and the chlorophyll a/b ratio was kept at 2 under Cr 6 stress (10-40 mg/L) (Yang et al. 2001).Sun and Wang (1985), however, reported that the chlorophyll a/b ratio of macrophytes decreased as the concentration of Cd increased and that Fe3 could abate the increasing trend (Li et al. 1992). Heavy metals affected the function of PSI and PS II, and it was stronger with the latter (Yang et al. 1989). The chlorophyll proteins, which took protons for photosynthesis in PS II, were decomposed and decreased under Cd stress. The sub-microstructure of chloroplast was changed and the membrane system was destroyed. Therefore, the capacity of taking protons declined and the photosynthesis function was influenced (Peng and Wang 1991). The photosynthesis of woody plants decreased under pollution with Cd from the atmosphere before the observed symptoms had occurred (Huang and Zhang 1986). Thus, the photosynthetic yield would be one of the indicators for air pollution.

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Yang and He 1995a, Yang et al. 1999a, 2001). Most of the effects are inhibitory. Cd reduced the activity of nitrate reductase in O. javanica (Xu and Shi 2000), but the activity of nitrate reductase in H. dubia and B. schreberi increased in low concentrations (4-8 mg/kg) of Cr 6+solution and reduced in higher concentrations (16-32 mg/kg) of solution (Yang et al. 1999a, 2001). In the tonoplast of wheat, the ATPase, Ca2 and PPase declined rapidly under AI stress (He et al. 1999). All these findings suggest that heavy metals inhibit the nitrogen metabolism, respiration and nucleic acid metabolism, and show toxicity to plants.
1.4.3 Content of proteins and amino acids

1.4.2 Activity of enzymes

The content of malondialdehyde (MDA) in plants is an indicator of lipid peroxidation. Treated by Cd or Pb, MDA in wheat germinating seedlings' (Tritium aestivum L.) leaves, shoots and roots were significantly enhanced and accumulated (Luo 1999, Pang et al. 2001). The content of 02-" and MDA in B. schreberi were little higher by Cr 6+treatment, while the trend of changes in MDA was relatively similar with that of 02-. (Yang et al. 2001). The high rate of tissue autoxidation in leaves, which indicated lipid peroxidation of cellular membrane, was stimulated by endogenously active oxygen radicals (Luo 1999). Huang and Hong (1997) reported that the accumulation of MDA in the plant seedling was related to the concentration of Cd. It can be concluded that membrane peroxidation by overabundant free radicals is one of the serious impact of heavy metals, such as Cd and Cr, on plants. Superoxide dismutase (SOD), peroxidase (POD) and catalase (CAT) are important enzymes for plants adapted to environmental stress, they are called the plant protective enzymatic system. The harmonious interactions of the three enzymes make the balance of free radical production and elimination, and keep the level of free radicals in plants low to prevent the injury of cells by free radical. The activities of POD, SOD and CAT are usually enhanced by heavy metal stress such as Cd, Cr 6+, Hg, Ni, Pb and Fe in low concentrations (Dong 1999, Li et al. 1999b, Ma 2000, Pang et al. 2001, Wang et al. 1996, Wang et al. 1999, Yang et al. 1999a, Yang et al. 2001). But, as the concentration of heavy metals increases, the activities decrease. Treated by Pb, the activity of SOD in the shoot and roots of wheat seedlings were significantly enhanced, the activity of CAT in the root was also improved, but the degree was not bigger than that of SOD activity (Pang et al. 2001). It suggested that the membrane system was damaged by Pb stress. With an increase in the concentration of Hg and/or Cd in soil, the activity of CAT in leaves of tobacco decreased, the activity of SOD increased first and decreased afterwards, and the activity of POD increased (Yan et al. 1997). Treated by Cr6%the activities of POD of B. schreberi and H. dubia were enhanced with the raising concentration of Cr 6+(Yang et al. 1999a, 2001). Treating the seedling of Trapa bispinosa L. by using different concentrations of Cd and Hg, Cd could initially induce the activity of SOD and POD to rise, but the activity declined sharply with extending time and increasing concentrations; while the activity of SOD and POD treated with Hg changed relatively smoothly, where the activity of POD rose continually when treated with 5 and 10 umol/ L Hg (Li et al. 1999b). Ni stimulated the activity of POD in rice seedlings (Wang et al. 1999) and Hg, Cr, Ni, Fe stimulated activity of CAT of Spirodela polyrrhiza Schleid (Dong 1999). On the other hand, Ni inhibited POD with a significantly negative relationship in wheat (Ma 2000) and Pb inhibited the activity of CAT of S. polyrrhiza (Dong 1999). Zn showed a synergism with Cd to enhance the activity of POD of Oenanthe javanica (Blume) DC (Xu and Shi 2000). In spite of SOD, POD and CAT, heavy metals also affect the activities of other enzymes such as alcohol dehydrogenase (ADH) (Lu and Wang 1998), amylase (Hong et al. 1991), DNase, RNase (Duan and Wang 1992), proteinase (Chen and Gong 1996) and nitrate reductase (Xu and Shi 2000,

Hong et al, (1991) and Li et al. (1992) reported that the dissolubility of proteins increased under Cd stress, which might be a detoxifying mechanism (e.g. Cd-protein produced to reduce the toxicity of Cd). On the other hand, the results of Qin et al. (1994) showed that the dissolubility of proteins of B. chinensis seedlings decreased with an increase in Cd concentration higher than 0.1 mg/L. The polypeptide composition of B. schreberi was degraded under Hg and Cd treatment, and the effect of Hg was more significant than that of Cd (Chen et al. 1999). Under a lower stress with Cd (lower than 20 mg/L), the contents of proline increased little in wheat seedlings, but increased higher under concentrations of 50 and 100 mg/L (Hong et al. 1991). This also occurred in B. chinensis seedlings (Qin et al. 1994). Proline is an important substance for infiltrative calibration, its accumulation was adapted to the environmental stress (Tang 1984). More studies should be done to show the potential of proline as an indicator for assaying the effect of environmental stress on plants.
1.4.4 Effects on absorption of nutrients

The hydroponical experiment of oat showed that the absorption capacity of K and Mg declined in suspended cultivated cells, and the absorption of Ca, Fe and Zn rose by Cd pollution. However, absorption of Zn declined in higher concentrations of Cd solution (Xu and Yang 1995). Wang (1990) reported that Cd significantly inhibited maize seedlings from absorbing N, P and Zn and enhanced the absorption of Ca. Cd also affected the absorption of Mn and Zn by roots of B. chinensis seedlings (Qin et al. 1994), inhibited the absorption of Fe, Mn, Cu, Zn, Ca and Mg by ryegrass (Lolium perenne), maize (Zea mays), shamrock (Trifolium repens) and cabbage (B. oleracea var. capitata) and increased the absorption of P (Yang et al. 1998). Those resuits show that Cd inhibited the absorption of N, K, Mg, Mn by plants. The effects on absorptions of P, S, Ca, Zn, Fe are more complicated are related to plant species and environmental stress, pH, elements.
2 Heavy Metal Bioavailability and Factors Influencing its Effects

The bioavailability and effects of heavy metals on plants are affected by many factors, such as organic substances, fertilization, plant species and so on.

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nism and synergism. Determination of heavy metals in the rice showed the content of Pb, Cd and Cr decreased by using low concentrations of Se, Se revealed an antagonism to the heavy metals (Tan et al. 2000). The results of Xia and Mu (1984) showed the effects of Cd, Pb, Zn on tobacco and wheat, and the interaction depended on the content of those heavy metals in the soil. Xu and Shi (2000) reported that Cd reduced the activity of nitrate reductase in O. javanica, Zn showed an antagonism with Cd when Wzn/Wcd>l/2, and synergism when WzffWca <1/2.
2.4 Fertilization

2.1

Organic substances

Yang et al. (2000) reported that organic and amino acids (such as citric acid, tartaric acid, oxalic acid, succinic acid, aspartic acid and glutamic acid) excreted by the roots of plant formed soluble complexes with heavy metals and increased the mobility of such heavy metals as Cd, Cu, Pb and Zn in soil. Chelators EDTA and DTPA were added to the nutrient solutions, the uptake rates of Zn, Cu, and Mn by Thlaspi caerulescens J and C Presl were significantly decreased (Shen et al. 1998). The growth of B. chinensis seedlings was inhibited by 200 mg/L CdCI2, when 10 mg/L LaGly was used to spray the plant one time, the damage effect of Cd was reduced. (Zhou et al. 1997).
2.2 pH

pH impacts the behavior of heavy metals. Acid rain might reduce the content of heavy metals in soil (Meng and Li 1998) and increases the content of heavy metals in leachate. The effects of leachate on plants increased as the duration and initial acidity of leaching (Lan et al. 1996). Studies on the bioavailability of Cd in plough horizons showed that the uptake of Cd by ryegrass increased with a decline in pH and declined with an increase of pH, and the plant available sources of Cd mainly came from the soil exchangeable Cd as well as Cd weakly bound to organic substances (Zhu and Shao 1997).
2.3 Elements

Through continuous composting, the contents of heavy metals in municipal waste did not become reduced, but the bioavailable contents for plants were seen to decline (Jiang 1999). Fertilizing the highway greenbelt by the composting of sludge showed no more accumulation of heavy metals in plants (Xue et al. 2000) and bioavailablity contents of heavy metals were decreased by complex cornposting. Generally, there are more organic carbons and, with a higher pH, there are lower bioavailablity contents of heavy metals in the composted fertilizer (Guo et al. 1995). In bio-solids used as fertilizer, most of the heavy metals were combined with organic carbon and carbonate, the mobility was declined and also related to pH, elements in soil and characteristics of the organic substances ('fang et al. 1997, Wen and Lu 1999). Therefore, using plants to remediate the municipal waste solids is possible (Hu 1996).
2.5 Plant species

Effects of heavy metals on the growth, physiological and biochemical characteristics of plants affect by other metal elements, as well as influencing the accumulation of heavy metals by plants. Some elements affect the absorption of heavy metals in plants. Fu et al. (1996) reported that the interaction of Zn and Cd on the absorption by rape seed seedlings (Brassica rape). When the content of Zn was lower than 25 mg/kg DW, Zn showed a synergism with the absorption of Cd. On the other hand, when the content of Zn was higher than 25 mg/kg DW, Zn showed an antagonism with Cd. With a modifying treatment using fertilizers with Ca, Mg and P, the migration and accumulation of heavy metals like Cd, Pb and Zn in the soil were retained, the accumulation of Cd and Pb in rice and wheat was reduced 31.5-55.0% and 23.4-57.8%, respectively, and that of Cu and Zn were also declined (Wang and Wu 1995). The reason was that fertilization changed the chemical form of heavy metals in the soil, their carbonates increased and the bioavailable contents declined. Studies also showed an interaction of P with the Zn and Cd in plants, the accumulation and transport of Zn and Cd from roots to above ground parts in plants raised by increasing the content of P in their media, and the influence was changed along with the characteristics of soil, plant species and environmental conditions (Yang et al. 1999b). The interaction of heavy metals with nutrient cations in soil is mostly antagonistic, while antagonistic or synergistic with nutrient anions, depending on soil properties (Tu et al. 1997). The effects of heavy metals on plant are also influenced by other elements, the interactions of which include antago-

The effects of Cd and Pb in soil on rice and cotton indicated that the ability of the geneticallymodified cotton to resist metal damage is stronger than that found for common cotton under the same conditions. Compared with cotton's absorbing ability at the same treated level, the absorption of Cd and Pb in rice leaves was lower (Qin et al. 2000). Leguminous (A. confusa, O. pinnata) and herbaceous (Vetiveria zizanioides Linn., Cynodon dactylon Linn.) species were more resistant to heavy metals and demonstrated a better purifying ability for leachate pollution (Jiang et al. 2001). Thus, these species should be considered as potential vegetation for landfill site remediation. Hydrilla verticillata L.f. Royle and Nympboicles peltatum were more resistant to Cd and Zn than Potamogeton nulaianus (Li et al. 2000). Therefore, selecting more highly resistant plants for phytoremediation in order to reduce the injury of heavy metals to plants in polluted areas is also a research point to be taken into account for phytoremediation.
2.6 Others

Fungi VA growing with plants enhances the resistance of the plant to heavy metals, and the resistance differs according to the VA fungi species, plant species and environmental conditions (Tang 1998). Tao et al. (1997) also reported that VA-mycorrhizal (G. mosseae) reduced the effects of Zn on red clover (Trifolium pratense) and increased the absorption of P for plant growth. Zhao and Mo (1997) exposed garlic in Cd solution and showed that ascorbic acid and molysite could reduce the

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toxicity of Cd to the root tips. Ascorbic acid can remove free radicals, and restore the function of membranes, enzymes and DNA to increase the synthesis of proteins and resistant proteins. Therefore, it also plays a role in detoxification. The ectomycorrhizal fungus Suillus bovines, however, increased the content of Cu and Zn in Pinus sylvestris (Huang et al. 2000). The bioavailability of Cd in soil is also affected by the redox potential. The redox potential increased from -150 to 200 mV, the exchangeable Cd decreased and the reductive form of Cd was increased (Suet al. 2000). In reductive soil, the deposition of CdS was induced so that the concentration of Cd decreased in the soil solution and plants uptook less of the heavy metals (Chen 1981).In the case of droughts and oxidized conditions, the absorbable Cd in the soil increased and rice (Oryza sative L.) accumulated more Cd in the organs, from 0.14 to 0.45 mg/kg DW (Chen et al. 1985). Chloride influences the bioavailability of Cd and demonstrates an antagonistic role on the toxicity of Cd in the soil (Suet al. 2000).
3 The Resistant Reaction of Plant to Heavy Metals and its Molecular Mechanisms

Another kind of substance induced for heavy metal detoxification is phytochelatin (PC). PC is not the direct product of gene translation, but a peptide synthesized as a substrate of glutathione (GSH), which is catalyzed by phytochelatin synthase (Zhang et al. 1999), the molecular weight of PCs are 2-4 KD and the chemical form is usually (r-GluCys)nGly(n=2-11). PCs were identified in snakewood, tobacco, navy beans, maize, tomatoes, broccoli and wheat (Li and Yu 1990). PC combined amounts of heavy metals in these plants to abate the toxicity to its physiological activities. However, reports also showed that PC in tolerant plants was less than those found in un-tolerant plants (Yang and He 1995b). Therefore, metal binding proteins and PC are important mechanisms for some plant detoxification, but they are limited so that other undiscovered detoxifying mechanisms may perhaps exist in plants.
3.2 Enzyme and nucleic acid gene expression

Heavy metals have an impact on the growth of plants, On the other hand, plants also have mechanisms to detoxify heavy metals. The mechanisms are reviewed with regard to their individual aspects: i) Retard the absorption of heavy metals and reduce the content of heavy metals in plants and, therefore, abate the impact of heavy metals on the plant, ii) Store the absorbed heavy metals in trichomes of epidermis to avoid the direct effect of heavy metals on the mesophyll. iii) Precipitate and chelated heavy metals in special site in the plant for detoxification, iv) Rise the anti-oxidization enzyme activities and remove free radicals to prevent the damage of free radicals to the plant; generally, under heavy metal stress, many free radicals are produced, v) Produce many kinds of proteins, which are induced by heavy metals, to resist the impact of environmental stress to the plant (Zhang et al. 1999). The molecular mechanism studies focus on the following fields.
3.1 Induced proteins and peptides

Duan and Wang (1998) studied the expression of lacti-dehydrogenase (LDH) of beans (Vicia faba L.) under the stress of Pb, Cd, Hg. There were different expressions of five isoenzymes at different dosages and they came to the conclusion that LDH was to be found in different forms to maintain the enzyme activities and to avoid injury resulting from the heavy metals. In wheat, alcohol dehydrogenase (ADH) gene expression was changed on two levels: RNA and enzymatic activities under exposed Pb and Cd for 45 hrs, and the changes were similar (Lu and Wang 1998). The change in ADH gene expression is the first response of plants to heavy metal pollution. Meng et al. (1998b) also studied the changes of protein gene expression in wheat seeds in Pb/Zn tailing areas, and found that the transcriptional quantities were different in different species, even in different cultivars of the same species, so that the changes might affect the micro-evolution of wheat under longterm heavy metal pollution. Cai et al. (1998) isolated seven different cDNA families from Hg-treated beans (Phaseolus vulgaris L.) by employing differential screening using cDNAs derived from treated plants and controls. Hg induced PvSR2 protein gene and PR protein gene expression. Northern blot analysis revealed a low level of transcripts of polyubiquitin in unstressed bean leaves, but the gene expression was strongly stimulated by heavy metals (Cai and Zhang 1999). Hg, Cd, As, Zn and Cu strongly induced the DNaJ-like protein gene expression. The various gene products might function to protect cells from heavy metal stress (Cai and Zhang 2000). Gene gap change, gene mutation and gene exchange are sources of the anti-pollution genes in plants; under the strong pollution, the anti-pollution genes are widely spread and microevaluated (Duan 1995).
4 Conclusion

Small molecular weight organic acid can chelate heavy metals (Yang et al. 2000), and metal-binding proteins or metallothionein are perfect for chelating heavy metals (Zhang et al. 1999). He and Luo (1991) extracted Cd-binding proteins in maize, the ratio of protein to Cd was 1:3. Yang and Wang (1985) reported metal-binding proteins could combine 40-50% of Cd, which entered into the cell. The formation of Cd-binding proteins limited the behavior of Cd and abated the injury of Cd to plants. Ma et al. (1997) identified metallothionein-like protein and its gene in Festuca rubra. These metal-binding proteins were also identified and/or purified from rice, beans, broccoli, tobacco, with the molecular weights being from 3.1 to 33.1 KD (Li and Yu 1990). Therefore, it is possible and feasible to use metallothiopeptides of the water hyacinth (Eichhornia crassipes L.) root as an indicator to assay the heavy metal pollution in water bodies (Wang et al. 1994).

Heavy metals in soil, water and atmosphere, where plants are living are seen to demonstrate interactions between these heavy metals and the plants. On the one hand, heavy metals show negative effects on plants by inhibiting the growth, damaging the structure, affecting the physiological and biochemical activities and decreasing the functions of the plants.

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The effects and bioavailability of heavy metals depend on many factors including environmental conditions such as pH, species of elements, and organic substances in the media as well as fertilization and the individual plant species. On the other hand, plants have their own mechanisms of resistance against the negative effects of heavy metals, by combining heavy metals with proteins and developing enzymes and nucleic acids to detoxify heavy metal pollution. These mechanisms are integrated to protect the plants against injury by heavy metals. Thus, the effects of heavy metals on plants are revealed in several aspects, and the plants show many kinds of resistance mechanisms.
5 Recommendations and Outlook

Review Articles
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To avoid of the negative effects of heavy metals on plants, the resistance mechanisms should be studied further, especially the molecule mechanisms and the role of glutathione (GSH) on the detoxification of heavy metals. This would help to benefit the selection and cultivation of plants for heavy metal phytoremediation. More highly resistant plants can be used to remediate the pollution area, which is the basic idea of green and environmentally-friendly phytoremediation techniques. The bioavailability of heavy metals to plants is dependent on two different aspects, too. There are two different strategies to manipulate the bioavailability of heavy metals. One is to decrease the bioavailability of heavy metals in paddy, vegetable fields and farmlands to reduce the accumulation of heavy metals in crops, vegetables, fruits and pasturages. In contrast, one involves increasing the bioavailability of heavy metals for plants to take up much more heavy metal from soil and water in order to clean the environment, and this is the choice used for heavy metal phytoremediation. Therefore, to understand the bioavailability of heavy metals is helpful both for cultivating crops and for developing phytoremediation techniques.
Acknowledgement. The author is very grateful to Prof. Dr. Wolfgang Grosse, Institute of Botany, University of Cologne, Germany, for his supervision and first review of the manuscript, also to Prof. Dr. Zhenbin Wu, Institute of Hydrobiology,The Chinese Academy of Sciences (CAS), China, for his support. This paper is supported by the Max-PlanckGesellschaft/CAS Exchange Program, Dawn Plan of Wuhan City, China (20005004044), and KIP Key Project of CAS (KSCX2-SW-102).

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Received: May 31 st, 2002 Accepted: November 12th, 2002 OnlineFirst: November 18th, 2002

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