Nickel toxicity in plants: the physiological relationship existing between plants and the serpentine soils on which they grow
Crooke, William Macgregor
The occurrence of nickel -toxic serpentine soils at Whitecairns, Aberdeenshire, led to an investigation of the effects of excess nickel on plants, together with a study of the soil factors affecting nickel absorption. The oat plant was selected as a suitable indicator plant. The results are summarised as follows:-1. Nickel, in comon with other heavy metals, induces iron deficiency when supplied in excess to plants, which vary in their tolerance to the toxicity. In oat plants, which are particularly sensitive, white stripes or bands of necrotic tissue are produced in addition to the chlorosis associated with iron deficiency. The chlorosis responds to painting or spraying with solutions of iron salts whereas the necrosis does not.2. Examination of nickel -toxic oat tissue by means of autoradiographs has shown that iron is low in the chlorotic areas and absent in the necrotic patches. Analysis of oat leaves from plants growing on the toxic serpentine soils confirmed these findings although some iron was still detected in the necrotic tissue, where in general, nutrients were at a lower level than in the rest of the leaf, suggesting a migration of nutrients out of this dying tissue.3. The absorption of nickel by young oat plants increases rapidly from germination for about 30 days when the concentration in the tissues reaches a maximum and thereafter starts to decrease slowly. The concentration of iron, on the other hand, starts at a high level in the young plants and falls only slightly with age. This change in rate of absorption of nickel is accompanied by change in the (visual) toxicity symptoms. Up till 50 days young leaves unfold chlorotic whereas after that time they emerge a normal green colour. Basal and intermediate leaves are necrotic but seldom chlorotic. When the nickel -iron ratio in the plant is plotted against time, the maximum point on the curve coincide . in point of time with the observed change in symptoms. The changes produced by nickel in the uptake of major nutrients were also followed. The concentrations of iron and phosphor were always lower in nickel -toxic than in control plants, whereas that of calcium was always higher. Magnesium and potassium content were not dissimilar in both types of plant at the same stage of growth. The change in concentration of the major nutrients in the growing plant were probably not a reflection of nickel treatment, but rather of normal metabolic processes in the plant, associated with the translocation of nutrients to the developing grain. In mature oat plants, nickel concentrates in the grain, more in young tissue than in old, and more in leaves than in stems.4. The visual symptoms produced i.n plants by excess nickel result from an upset in iron metabolism. Experiments were therefore designed to examine this antagonism. It was found that increase in iron supply reduced toxic symptoms and the uptake of nickel, although plants showing no visual symptoms still contained appreciable amounts of nickel. It was confirmed that a reciprocal relationship exists between the nickel and iron contents of the plant; the nickel content is reduced by high concentrations of iron in the nutrient solution and the iron content by nickel, the former being the more pronounced effect. The reduction in the degree of necrosis is related to a reduced nickel content in the plant while that of chlorosis is related to the nickel-iron ratio in the plants. The absolute amounts of iron and nickel in the substrate rather than the iron status of the plant determine the degree of symptoms and uptake of nickel, although the ratio of nickel to iron in the substrate also plays a part in deciding how severely plants will be affected Narrow ratios are associated with severe symptoms; while for the same nickel -iron ratio, symptoms increase in severity as nickel in the nutrient solution increases. The degree of symptoms and the nickel-iron ratio in the plant are connected linearly. The external nature of the nickel -iron antagonism was confirmed in a split -root experiment using tomato as indicator plant.5. The absorption of nickel by oat plants was studied in solution culture and is found to increase with increasing pH; but this increased absorption of nickel is not dimply due to decreased availability of iron as a result of the high pH of the cultures. The same degree of necrosis is found over pH range 4 - 7 but chlorosis is more severe above pH 6. In the field, increase in soil pH brought about by liming, results in lowered absorption of nickel and reduced toxic symptoms, suggesting a reduction in the availability of the soil nickel. The beneficial effect is due solely to the pH change involved and is not dependent on an increased calcium status, since sodium carbonate will produce the same result. It is found that the amount of soil nickel extract- able by N-ammonium acetate falls with increase in soil pH. Laboratory studies on the recovery of nickel added to soils of varying pH (produced by the addition of either calcium or sodium carbonate) gave the same result. In a series of pot - culture experiments using toxic soils. limed with either calci or sodium carbonate to give a range of soil pHs, the uptake o nickel by the plants and the degree of symptoms observed agreed well with the "exchangeable" nickel removed from the soils after the experiment by leaching with ammonium acetate.6. Field observations indicated that liming reduced the toxic symptoms in oats while applications of phosphorus fertilizers made symptoms worse. Nitrogen also improved growth while potash and magnesium applications had little effect. Sand- culture experiments have been used to examine the effect of variation in major nutrient supply on nickel toxicity symptoms and uptake of nickel. Increase in the concentration of cations in the nutrient solution was found to affect the toxic symptoms and nickel uptake markedly. The largest beneficial effect was obtained with calcium or magnesium and least with potash. In the absence of pH changes, which accounted for differences in uptake of nickel from soils, the effects found here must be due to direct competition for absorption between the cations concerned. Increase in rate of phosphorus supply was still found to increase symptom degree and uptake of nickel. The simplest hypothesis to account for this effect would involve reduction in the level of iron absorbed and translocated, and as has been pointed out earlier, a lowered iron status in the plant would result in increased nickel toxicity. Nickel was found to increase the concentration of calcium in the tissues but from the available data no explanation for this phenomenon can be offered.7. Molybdenum has been found by some workers to cure the iron deficiency chlorosis induced by certain heavy metals. No definite indication of any such beneficial effect was noted when molybdenum was supplied to nickel -toxic oat plants.8. The soils from the most severely affected area at Whitecairns are characterised and compared with several uncultivated serpentine soils from other parts of Aberdeenshire. The mineral soils from Whitecairns are found to be generally higher in nickel than other Aberdeenshire serpentine soils. The Whitecairns soil which produced the most severe cases of nickel toxicity, is a very peaty soil occurring in a lowlying basin at the foot of a slope of mineral serpentine soil. Nickel leached out of this mineral soil accumulates and is firmly retained by the peaty soil. There is some evidence that the nickel in this soil is held on the organic matter by some form of loose chelate bonding from which it can be displaced by extraction with a 1% solution of zinc sulphate although not by dilute acetic acid.9. Two forms of iron were used in these plant culture studies; ferric citrate and a chelate form employing ethylene-diamine tetra-acetic acid (EDTA). Both appeared equally good sources of iron and when certain aspects of the work were repeated using the chelate form identical results were obtained. There was no indication of any exchange between ionic nickel present in the nutrient solution and the chelate form of iron. Further evidence of this was supplied indirectly when it was found that nickel complexed by EDTA was unavailable to oat plants. The level of chelated nickel supplied was increased to 25 ppm. without any nickel being absorbed by the plants. This level of nickel would be very toxic to oats if supplied in ionic form. The availability of other heavy metal chelates also showed interesting differences.10. An existing colorimetric method for the estimation of nickel was successfully adapted to permit of its use on plant and soil extracts.