Comparison of mercury, lead and arsenic with respect to genotoxic effects on plant systems and the development of genetic tolerance

Abstract

Metals can, when present in excess, or under wrong conditions, and in the wrong places, produce errors in the genetic information system. The present review is limited to three examples of heavy metal genotoxicants, namely arsenic (As), lead (Pb) and mercury (Hg) on plant systems. Exposure to lead is mainly through atmospheric pollutants, to mercury through soil and to arsenic through drinking water. Toxic metal ions enter cells by means of the same uptake processes as essential micronutrient metal ions. The amounts of metal absorbed by a plant depend on the concentrations and speciation of the metal in the soil solution, its movement successively from the bulk soils to the root surface, then into the root and finally into the shoot. Excessive concentrations of metals result in phytotoxicity through: (i) changes in the permeability of the cell membrane; (ii) reactions of sulphydryl (-SH) groups with cations; (iii) affinity for reacting with phosphate groups and active groups of ADP or ATP; and (iv) replacement of essential ions. Mercuric cations have a high affinity for sulphydryl groups and consequently can disturb almost any function where critical or non-protected proteins are involved. A mercury ion may bind to two sites of a protein molecule without deforming the chain, or it may bind two neighbouring chains together or a sufficiently high concentration of mercury may lead to protein precipitation. With organomercurials, the mercury atom still retains a free valency electron so that salts of such compounds form a monovalent ion. The effect of lead depends on the concentration, type of salts and plant species involved. Though effects are more pronounced at higher concentrations and durations, in some cases, lower concentrations might stimulate metabolic processes. The major processes affected are seed germination, seedling growth, photosynthesis, plant water status, mineral nutrition, and enzymatic activities. The phytotoxicity of arsenic is affected considerably by the chemical form in which it occurs in the soil and concentration of the metalloid. Due to its chemical similarity to phosphorus, arsenic participates in many cell reactions. Specific organo-arsenical compounds have been found in some organisms and arsenic has been reported to replace phosphorus in the phosphate groups of DNA. In view of the variety of reactions in plants that involve sulphydryl groups and phosphorus, arsenites and arsenates may interfere with physiological and biochemical processes which constitute growth in a number of ways. Mercury, lead and arsenic are effective mitotic poisons (turbagens) at particular concentrations, due to their known affinity for thiol groups and induce various types of spindle disturbances. The clastogenic effects are S-dependent. The availability of cations affect the number of aberrations produced quantitatively. Effects of metallic salts are related directly to the dosage and duration of exposure. Plants, following lower exposure, regain normalcy on being allowed to recover. Studies on genotoxicity of metals discussed in this review showed that genotoxic effects could be in part responsible for metal phytotoxicity, deserving further examination to elucidate the underlying mechanisms. The most noticeable and consistent effect of mercurials was the induction of c-mitosis resulting in the formation polyploid and aneuploid cells, and c-tumours. Inorganic salts of lead induced numerous c-mitoses together with strong inhibition of root growth and lowering of mitotic activity. As(III) is a weak mutagen but potent comutagen. Genotoxic evaluation of chemical mixtures from soil containing arsenic as component by Tradescantia micronucleus assay showed clastogenic effects, but not related specifically to arsenic. Plants growing on metal-contaminated sites need to develop some degree of tolerance to metal toxicity in order to survive. Since all plants contain at least some metal in their tissues, they clearly are incapable of completely excluding potentially toxic elements, but simply of restricting their uptake and/or translocation. The mechanisms for metal tolerance proposed are: (a) metal sequestration by specially produced organic compounds; (b) compartmentalization in certain cell compartments; (c) metal ion efflux; (d) organic ligand exudation. Inside cells, proteins such as ferritins and metallothioneins, and phytochelatins, participate in excess metal storage and detoxification. When these systems are overloaded, oxidative stress defence mechanisms are activated. Bacterial plasmids encode resistance systems for toxic metal ions including mercury, lead and arsenic. Chromosomal determinants of toxic metal resistance are also known. For mercury and arsenic, the plasmid and chromosomal determinants are basically the same. The largest group of metal resistance systems functions by energy-dependent efflux of toxic ions. Mercury-resistant bacteria have genes for the enzymes mercuric ion reductase and organomercurial lyase, which are often plasmid-encoded, and more rarely by transposons and bacterial chromosome. All mercury resistance genes are clustered into an operon. The expression of the operon is regulated and is inducible by Hg(II). Lead tolerance in Festuca ovina is an inherited characteristic, evolved by the production of compounds within the plants, specifically for protection against the toxic effects of heavy metals. A small number of genes are probably producing the major effects, and modifiers for dominance are present, which are probably affected by the genome as a whole. Arsenic tolerance appears to be genetically controlled in a fairly simple Mendelian manner but the specific mechanisms may be one or several, acting in cohesion. The ars operon provides resistance to arsenicals and as well antimonials. Arsenic-resistant bacterial and yeast strains may prove an important tool for identifying the genes for arsenic transporters in higher plants.