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Mercury Toxicity in Plants

Manomita Patra and Archana Sharma
Botanical Review
Vol. 66, No. 3 (Jul. - Sep., 2000), pp. 379-422
Published by: Springer on behalf of New York Botanical Garden Press
Stable URL: http://www.jstor.org/stable/4354375
Page Count: 44
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Mercury Toxicity in Plants
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Abstract

Mercury poisoning has become a problem of current interest as a result of environmental pollution on a global scale. Natural emissions of mercury form two-thirds of the input; man-made releases form about one-third. Considerable amounts of mercury may be added to agricultural land with sludge, fertilizers, lime, and manures. The most important sources of contaminating agricultural soil have been the use of organic mercurials as a seed-coat dressing to prevent fungal diseases in seeds. In general, the effect of treatment on germination is favorable when recommended dosages are used. Injury to the seed increases in direct proportion to increasing rates of application. The availability of soil mercury to plants is low, and there is a tendency for mercury to accumulate in roots, indicating that the roots serve as a barrier to mercury uptake. Mercury concentration in aboveground parts of plants appears to depend largely on foliar uptake of Hg0 volatilized from the soil. Uptake of mercury has been found to be plant specific in bryophytes, lichens, wetland plants, woody plants, and crop plants. Factors affecting plant uptake include soil or sediment organic content, carbon exchange capacity, oxide and carbonate content, redox potential, formulation used, and total metal content. In general, mercuty uptake in plants could be related to pollution level. With lower levels of mercury pollution, the amounts in crops are below the permissible levels. Aquatic plants have shown to be bioaccumulators of mercury. Mercury concentrations in the plants (stems and leaves) are always greater when the metal is introduced in organic form. In freshwater aquatic vascular plants, differences in uptake rate depend on the species of plant, seasonal growth-rate changes, and the metal ion being absorbed. Some of the mercury emitted from the source into the atmosphere is absorbed by plant leaves and migrates to humus through fallen leaves. Mercury-vapor uptake by leaves of the C3 species oats, barley, and wheat is five times greater than that by leaves of the C4 species corn, sorghum, and crabgrass. Such differential uptake by C4 and C4 species is largely attributable to internal resistance to mercury-vapor binding. Airborne mercury thus seems to contribute significantly to the mercury content of crops and thereby to its intake by humans as food. Accumulation, toxicity response, and mercury distribution differ between plants exposed through shoots or through roots, even when internal mercury concentrations in the treated plants are similar. Throughfall and litterfall play a significant role in the cycling and deposition of mercury. The possible causal mechanisms of mercury toxicity are changes in the permeability of the cell membrane, reactions of sulphydryl (-SH) groups with cations, affinity for reacting with phosphate groups and active groups of ADP or ATP, and replacement of essential ions, mainly major cations. In general, inorganic forms are thought to be more available to plants than are organic ones. Plants can be exposed to mercurials either by direct administration as antifungal agents, mainly to crop plants through seed treatment or foliar spray, or by accident. The end points screened are seed germination, seedling growth, relative growth of roots and shoots, and, in some case, studies of leaf-area index, internode development, and other anatomical characters. Accidental exposures occur through soil, water, and air pollution. The level of toxicity is usually tested under laboratory conditions using a wide range of concentrations and different periods of exposure. Additional parameters include biochemical assays and genetical studies. The absorption of organic and inorganic mercury from soil by plants is low, and there is a barrier to mercury translocation from plant roots to tops. Thus, large increases in mercury levels in soil produce only modest increases in mercury levels in plants by direct uptake from soil. Injuries to cereal seeds caused by organic mercurials has been characterized by abnormal germination and hypertrophy of the roots and coleoptile. Mercury affects both light and dark reactions of photosynthesis. Substitution of the central atom of chlorophyll, magnesium, by mercury in vivo prevents photosynthetic light harvesting in the affected chlorophyll molecules, resulting in a breakdown of photosynthesis. The reaction varies with light intensity. A concentration and time-dependent protective effect of GSH seems to be mediated by the restricted uptake of the metal involving cytoplasmic protein synthesis. Plant cells contain aquaporins, proteins that facilitate the transport of water, in the vacuolar membrane (tonoplast) and the plasma membrane. Many aquaporins are mercury sensitive, and in AQP1 a mercury-sensitive cysteine residue (Cys-189) is present adjacent to a conserved Asn-Pro-Ala motif. At low concentrations mercury has a toxic effect on the degrading capabilities of microorganisms. Sensitivity to the metal can be enhanced by a reduction in pH, and tolerance of mercury by microorganisms has been found to be in the order: total population > nitrogen fixers > nitrifiers. Numerous experiments have been carried out to study the genetic effects of mercury compounds in experimental test systems using a variety of genetic endpoints. The most noticeable and consistent effect is the induction of c-mitosis through disturbance of the spindle activity, resulting in the formation of polyploid and aneuploid cells and c-tumors. Organomercurials have been reported to be 200 times more potent than inorganic mercury. Exposure to inorganic mercury reduces mitotic index in the root-tip cells and increases the frequency of chromosomal aberrations in degrees directly proportional to the concentrations used and to the duration of exposure. The period of recovery after removal of mercury is inversely related to the concentration and duration of exposure. Bacterial plasmids encode resistance systems for toxic metal ions, including Hg2+, functioning by energy-dependent efflux of toxic ions through ATPases and chemiosmotic cation-proton antiporters. The inducible mercury resistance (mer) operon encodes both a mercuric ion uptake and detoxification enzymes. In gram-negative bacteria a periplasmic protein, MerP, an inner-membrane transport protein, MerT, and a cytoplasmic enzyme, mercuric reductase, the MerA protein, are responsible for the transport of mercuric ions into cells and their reduction to elemental mercury, Hg(II). In Thiobacillus ferrooxidans, an acidophilic chemoautotrophic bacterium sensitive to mercury ions, a group of mercury-resistant strains, which volatilize mercury, has been isolated. The entire coding sequence of the mercury-ion resistance gene has been located in a 2.3 kb fragment of chromosomal DNA (encoding 56,000 and 16,000 molecular-weight proteins) from strain E-15 of Escherichia coli. Higher plants and Schizosac-charomyces pombe respond to heavy-metal stress of mercury by synthesizing phytochelatins (PCs) that act as chelators. The strength of Hg(II) binding to glutathione and phytochelatins follows the order: $\gamma {\rm Gly}\text{-}{\rm Cys}\text{-}{\rm Gly}<(\gamma {\rm Glu}\text{-}{\rm Cys})_{2}{\rm Gly}<(\gamma {\rm Glu}\text{-}{\rm Cys})_{3}{\rm Gly}<(\gamma {\rm Glu}\text{-}{\rm Cys})_{4}{\rm Gly}$. Suspension cultures of haploid tobacco, Nicotiana tabacum, cells were subjected to ethyl methane sulfonate to raise mercury-tolerant plantlets. ${\rm HgCl}_{2}\text{-tolerant}$ variants were selected from nitrosoguanidine (NTG)-treated suspension cell cultures of cow pea, Vigna unguiculata, initiated from hypocotyl callus and incubated with 18 $\mu {\rm g}/{\rm ml}\ {\rm HgCl}_{2}$. Experiments have been carried out to develop mercury-tolerant plants of Hordeum vulgare through previous exposure to low doses of mercury and subsequent planting of the next generation in mercury-contaminated soil. Phytoremediation involves the use of plants to extract, detoxify, and/or sequester environmental pollutants from soil and water. Transgenic plants cleave mercury ions from methyl-mercury complexes, reduce mercury ions to the metallic form, take up metallic mercury through their roots, and evolve less toxic elemental mercury. Genetically engineered plants contain modified forms of bacterial genes that break down methyl mercury and reduce mercury ions. The first gene successfully inserted into plants was merA, which codes for a mercuric ion reductase enzyme, reducing ionic mercury to the less toxic elemental form. MerB codes for an organomercurial lyase protein that cleaves mercury ions from highly toxic methyl mercury compounds. Plants with the merB gene have been shown to detoxify methyl mercury in soil and water. Both genes have been successfully expressed in Arabidopsis thaliana, Brassica (mustard), Nicotiana tabacum (tobacco), and Liriodendron tulipifera (tulip poplar). Plants currently being transformed include cattails, wild rice, and Spartina, another wetland plant. The problem of mercury contamination can be reduced appreciably by combining the standard methods of phytoremediation-removal of mercury from polluted areas through scavenger plants-with raising such plants both by routine mutagenesis and by genetic engineering. The different transgenics raised utilizing the two genes merA and merB are very hopeful prospects.

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