Physical And Chemical Properties Of Nickel And Its Role In Animal And Bacterial Systems

Nickel is a first-row transition metal with chemical and physical characteristics ideally suited to biological activity (18). Divalent nickel is the only oxidation state of nickel that is likely to be of any importance to higher plants. Nevertheless, Ni2+ forms a bewildering array of complexes with a variety of coordination numbers and geometries (19). Nickel readily binds, complexes, and chelates a number of substances of biological interest and is ubiquitous in all biological systems. Nickel is now known to be a functional constituent of seven enzymes, six of which occur in bacterial and animal systems, but not known to be active in plants, but the seventh enzyme, urease, is widely distributed in biology. The sensitivity of known biological nickel-complex equilibriums to temperature, concentration, and pH also make nickel an ideal element for the fine control of enzyme reactions (18).

14.3.1 Nickel-Containing Enzymes and Proteins

The field of nickel metallobiochemistry has seen tremendous growth over the preceding 10 years, and nickel is clearly a biologically important element in a diverse range of organisms. Indeed, it is highly likely that with the advent of molecular techniques to search for genetic and functional homology rapidly, the diversity of known functions of nickel in biology will increase substantially in the coming years. Advances in the field of bacterial and animal biology will rapidly flow to the plant sciences.

To date, seven nickel-dependent enzymes have been identified. Two of these enzymes have nonredox function (urease and glyoxylase), and the remaining five involve oxidation-reduction reactions (Ni-superoxide dismutase, methyl coenzyme M reductase, carbon monoxide dehydrogenase, acetyl coenzyme A synthase, and hydrogenase).

In all microorganisms that produce nickel-dependent metalloenzymes, there exist a number of proteins involved in nickel uptake, transport storage, and incorporation into the metalloenzyme. In bacteria, the transport of nickel into the cell involves two high-affinity transport systems, an ATP-dependent Nik family (Nik a-e) in Escherichia coli and a variety of nickel permeases (NixA, HoxN, etc.) in diverse species (17). Incorporation of nickel into the metalloenzyme involves a number of accessory proteins including metallo-chaperones (UreE, HypB, and CooJ) involved in nickel storage and in protein assembly (17).

Of the established nickel enzymes and proteins, urease is the sole nickel-specific enzyme known to function in plants; however, nickel-dependent hydrogenase also indirectly influences plant productivity through its role in nitrogen-fixing symbionts (20) and in leaf commensal bacteria (21). Currently, none of the bacterial proteins involved in nickel uptake and assimilation (NikA, NixA, UreE, etc.) is known to be present in plants. Interestingly, the hydrogenase and urease activities of leaf-surface symbionts are clearly inhibited when they colonize urease-deficient soybean mutants (21). The mechanism by which this inhibition occurs is unknown but may suggest that the urease-deficient mutants lack key nickel assimilatory proteins, thus preventing the transfer of nickel to the leaf-surface bacterial enzymes. This possibility would suggest that plants might contain nickel-dependent assimilatory proteins.

Nielsen reported the first description of a dietary deficiency of nickel in animals in 1970 for chickens and later for rats (Rattus spp.), goats (Capra hircus), sheep (Ovis aries), cows (Bos taurus), and mini pigs (Sus scrofa) (7). Nickel deficiency in these animals results in growth depression, physiological and anatomical disruption of liver function, and disruption of iron, copper, and zinc metabolism resulting in reduced levels of these enzymes in blood and various organs (22). Nickel deficiency also markedly reduces the activity of a number of hepatic enzymes, including several hydrogenases, urease, and glyoxylase, though a specific functional role for nickel in these enzymes in animals has not been determined.

One of the important and consistent findings from animal studies is that nickel deficiency induces iron deficiency, an observation that is also made in plants (15). In rats (22), and in sheep (23), nickel deprivation resulted in decreased iron uptake and reduced tissue-iron concentrations. Nielsen et al. (24) have suggested several possible roles for nickel in iron metabolism and oxidation-reduction (redox) shifts that draw upon the observation that nickel and iron are associated in a number of bacterial redox-based enzymes (17).

The suggestion that additional nickel-dependent enzymes and proteins are present in higher plants is supported by the observation that several of the known bacterial nickel-containing enzymes have analogs in plants and animals (including superoxide dismutase, glyoxylase, acetyl coenzyme A synthase, and hydrogenase). Our current failure to identify additional nickel-dependent enzymes in plants is likely a result of the relatively primitive state of plant enzymology, in contrast to bacterial enzymology, and the difficulty involved in research on complex organisms involving ultra-trace elements. The similarity between the effects of nickel deficiency in animals and plants also provides evidence of a common biological role for nickel in all organisms.

14.3.2 Essentiality and Function of Nickel in Plants

The first evidence of a response of a field crop to application of a nickel fertilizer was demonstrated in 1945 for potato (Solanum tuberosum L.), wheat (Triticum aestivum L.), and bean (Phaseolus vulgaris L.) crops (25). In these crops, the application of a dilute nickel spray resulted in a significant increase in yield. These experiments were conducted on the 'Romney Marshes' of England, a region that is well known for its trace mineral deficiencies, particularly of manganese and zinc. These experiments were conducted very carefully and excluded the possibility that the nickel applied was merely substituting for manganese, zinc, iron, copper, or boron, suggesting that the growth response was indeed due to the application of nickel. Interestingly, the soils of this region may be low in nickel since the conditions that limit manganese and zinc availability in these soils (acid sands of low mineral content) would also limit nickel availability to crops, and the concentrations of nickel provided were appropriate based on the current knowledge of nickel demand. These same soil types also dominate the region of southeast United States where Ni deficiency is now known to occur.

Mishra and Kar (26) and Welch (27) reviewed the evidence of the role of nickel in biological systems and cited many examples of yield increases in field-grown crops in response to the application of nickel to the crop or to the soil. The significance of these purported benefits of field applications of nickel is difficult to interpret since the majority of the reported experiments used very high nickel application rates. None of these reports considered the possibility that nickel influenced plant yield through its effect on disease suppression, nor was the nickel concentration in the crops determined. Indeed, prior to the availability of graphite-furnace atomic absorption spec-trophotometers and inductively coupled plasma mass spectrometers (in the mid-1970s), it was exceedingly difficult to measure nickel at the concentrations (<0.1 mg Ni kg"1 dry weight) later shown to be critical for normal plant growth. In the absence of information on tissue-nickel concentrations, it is impossible to conclude that the observed yield increases were the result of a correction of a nickel deficiency in the plant.

Clear evidence that nickel application benefited the growth of nitrogen-fixing species of plant was demonstrated by Bertrand and DeWolf (28), who reported that soil-nickel application to field-grown soybean (Glycine max Merr.) resulted in a significant increase in nodule weight and seed yield. The authors suggested that the yield increase was the result of a nickel requirement of the nitrogen-fixing rhizobia. A specific role for nickel in nitrogen-fixing bacteria is now well established with the determination that a nickel-dependent hydrogenase is active in many rhizobial bacteria (20) and is thus essential for maximal nitrogen fixation (29). Nickel is also known to be essential for nitrogen fixation of the free-living cyanobacterium, Nostoc muscorum C.A. Adargh, though the specific mechanism has not been determined (30).

A role for nickel in plant disease resistance has long been observed and has been variously attributed to a direct phyto-sanitary effect of nickel on pathogens, or to a role of nickel on plant disease-resistance mechanisms. Mishra and Kar (26) concluded that nickel likely acted to reduce plant disease by direct toxicity to the pathogen. Nickel, however, is not particularly toxic when applied directly to microorganisms, and Graham et al. (31) demonstrated that nickel supplied to the roots of cowpea (Vigna unguiculata Walp.) that contained only 0.03 mg Ni kg"1 dry weight effectively reduced leaf-fungal infection by 50%. Whether this effect was directly due to a role of nickel in plant defense reactions (possibly involving superoxide dismutase-mediated processes) or a consequence of the alleviation of deficiency-induced changes in nitrogen metabolites (urea, amino acids, etc.) is uncertain. Regardless of the mechanism, a positive effect of nickel supplementation on disease tolerance was clearly documented.

The discovery that nickel is a component of the plant urease in 1975 (3) prompted a renewed interest in the role of nickel in plant life. In 1977, Polacco (32) determined that tissue-cultured soybean cells could not grow in the absence of nickel when provided with urea as the sole nitrogen source. Subsequently, an absolute nickel requirement was demonstrated for tissue-cultured rice (Oryza sativa L.) and tobacco (Nicotiana tabacum L.) (26,27). This finding was followed in 1981 by a review of nickel in biology that suggested that leguminous plants might have a unique requirement for nickel (28).

Using a novel chelation chromatography technique to remove nickel as a contaminant from the nutrient media, Eskew et al. (9,33,34) and Walker et al. (11) demonstrated that, under nickel-deficient conditions, urea accumulated to toxic levels in the leaves of soybean and cowpea. Leaflet tips of nickel-deficient plants contained concentrations of urea as high as 2.4% dry weight. The accumulation of urea occurred irrespective of the nitrogen source used and was assumed to have occurred as a result of urease-dependent disruption of the arginine-recycling pathway. Eskew et al. (9) concluded that nickel was an essential element for leguminous plants though they did not demonstrate a failure of nickel-deficient plants to complete their life cycles. Recently, Gerendas et al. (12-14), in a series of elegant studies demonstrated a profound effect of nickel deficiency on the growth of urea-fed tobacco, zucchini (Cucurbita pepo L.), rice, and canola (Brassica napus L.), but observed no growth inhibition when nitrogen sources other than urea were used.

Confirmation that nickel was essential for higher plants was provided by Brown et al. (1), who demonstrated that barley seeds from nickel-deprived plants were incapable of germination even when grown on a nitrogen source other than urea. Significant restrictions in shoot growth of barley, oats, and wheat (Triticum aestivum L.) were subsequently demonstrated under nickel-deficient conditions when the plants were supplied with mineral nitrogen sources (15). Brown et al. (15) also observed a marked suppression in tissue-iron concentrations in nickel-deficient plants, a response that is also observed in nickel-deficient animals (7). Reductions in tissue-malate concentrations have also been observed in nickel-deficient animals and plants (15,24,35). Confirmation of the essentiality of Ni under field conditions was provided in 2004 by Wood et al. (2), who observed a marked and specific positive response to application of Ni fertilizer to pecan (Carya illinoinensis K. Koch) and other species (2) that could not be corrected with any other known essential element.

The demonstration of a role for nickel in diverse plant species, the presence of nickel in a discrete metabolic process, and the failure of plants to complete their life cycles in the absence of nickel, satisfies the requirement for the establishment of essentiality (4).

Although nickel has been accepted generally as an essential element, there is reason to be cautious about this conclusion, and some authors suggest that nickel may not fully satisfy the most stringent interpretation of the laws of essentiality primarily since its role in a specific essential metabolic function has not been identified. Furthermore, even though nickel has a clear role in metabolism, it is now clear that urease is not, by itself, essential for plant life as evidenced by the observation that urease-null soybean mutants can complete their life cycles (37). There has also been no independent replication of the effect of nickel on barley grain viability though Horak (36) did observe a marked increase in seed viability with the addition of nickel to pea (Pisum sativum L.) seeds grown in nickel-deficient soils.

Regardless of these apparent contradictions, nickel is still clearly required for normal plant metabolism. As a component of urease, nickel is required for urea and arginine metabolism, and both of these metabolites are normal constituents of plants (5). Nickel is also an essential component of hydrogenases involved in nitrogen fixation and other associative bacterial processes, and nickel clearly influences plant response to disease. Nickel is clearly a normal constituent of plant life.

Many of the reported effects of nickel on plant growth cannot be attributed solely to the role of nickel in urease, and many symptoms of nickel deficiency (disrupted iron and malate metabolism) are also observed in animals (7). It is likely, therefore, that additional nickel-dependent enzymes and proteins await discovery and will help resolve the remaining questions on the function of nickel in plants.

14.3.3 Influence of Nickel on Crop Growth

Many early reports of the role of nickel in agricultural productivity have been questioned since they did not adequately exclude the possibility that nickel was acting directly as a fungicidal element (27). Regardless of the many questionable reports, a compelling body of literature exists in which appropriate concentrations of nickel were applied or where the plant response is consistent with current knowledge of nickel functions including effects on nitrogen fixation, seed germination, and disease suppression (26,27,31,34,38,39).

The clearest agronomic responses to nickel have been observed when nitrogen is supplied as urea or by nitrogen fixation. The most illustrative example of the relationship between nickel and urea metabolism is provided from studies with foliar urea application and tissue-culture growth of plants. Plants without a supply of nickel have low urease activity in the leaves, and foliar application of urea leads to a large accumulation of urea and severe necrosis of the leaf tips (34). Nicoulaud and Bloom (40) observed that nickel, provided in the nutrient solution of tomato (Lycopersicon esculentum Mill.) seedlings growing with foliar urea as the only nitrogen source, significantly enhanced growth. The authors speculated that the effect of nickel was more consistent with its role in urea translocation than that on urease activity directly (40). This result is in agreement with the findings of Brown et al. (15), who suggest that nickel has a role in the transport of nitrogen to the seed thereby influencing plant senescence and seed viability.

The first demonstration of an agricultural Ni deficiency did not occur until 2004 (Wood et al., 2004), when it was observed in pecan (Carya illinoinensis). Nickel deficiency in pecan is associated with a physiological disorder 'mouse-ear' which occurs sporadically, but with increasing frequency, throughout the southeastern United States (portions of South Atlantic region) where it represents a substantial economic impact. In agreement with the results of Brown et al. (1), Ni deficiency in pecan results in a disruption of nitrogen metabolism and altered amino acid profiles (72).

The value of addition of nickel to Murashige and Skoog plant tissue-culture medium was shown by Witte et al. (41). These authors suggested that the lack of nickel and urease activity may represent a stress factor in tissue culture and recommended that the addition of 100 nM Ni be adopted as a standard practice. The benefits of adding nickel to solution cultures was also demonstrated by Khan et al. (42), who determined that a mixture of 0.05 mg Ni L_1 and 20% nitrogen as urea resulted in optimal growth of spinach (Spinacia oleracea L.) under hydroponic conditions.

14.4 DIAGNOSIS OF NICKEL STATUS 14.4.1 Symptoms of Deficiency and Toxicity

In legumes and other dicotyledonous plants, nickel deficiency results in decreased activity of urease and subsequently in urea toxicity, exhibited as leaflet tip necrosis (9-11). With nitrogen-fixing plants or with plants grown on nitrate and ammonium, nickel deficiency results in a general suppression in plant growth with development of leaf tip necrosis on typically pale green leaves (9,10) (Figure 14.1 and Figure 14.2). These symptoms were attributed to the accumulation of toxic levels of urea in the leaf tissues.

In graminaceous species (Figure 14.3), deficiency symptoms include chlorosis similar to that induced by iron deficiency (1), including interveinal chlorosis and patchy necrosis in the youngest leaves. Nickel deficiency also results in a marked enhancement in plant senescence and a reduction in tissue-iron concentrations. In monocotyledons and in dicotyledons, the accumulation of urea in leaf tips is diagnostic of nickel deficiency. In early or incipient stages of nickel toxicity, no clearly visible symptoms develop, though shoot and root growth may be suppressed. Acute nickel toxicity results in symptoms that have variously been likened to iron deficiency (interveinal chlorosis in

figure 14.1 Nitrogen-fixing cowpea seedlings (Vigna unguiculata Walp.) were grown for 40 days in nutrient solutions containing either 1 (left) or 0 |J,g L"1 (right) and supplied with no inorganic nitrogen source. In the absence of nickel, plants developed pronounced leaf tip necrosis and marked yellowing and growth stunting. The observed symptoms closely resemble those of nitrogen deficiency. (Photograph by David Eskew.) (For a color presentation of this figure, see the accompanying compact disc.)

figure 14.1 Nitrogen-fixing cowpea seedlings (Vigna unguiculata Walp.) were grown for 40 days in nutrient solutions containing either 1 (left) or 0 |J,g L"1 (right) and supplied with no inorganic nitrogen source. In the absence of nickel, plants developed pronounced leaf tip necrosis and marked yellowing and growth stunting. The observed symptoms closely resemble those of nitrogen deficiency. (Photograph by David Eskew.) (For a color presentation of this figure, see the accompanying compact disc.)

figure 14.2 Leaf tip necrosis in soybean plants (Glycine max Merr.) grown in nutrient solution provided with equimolar concentrations of nitrate and ammonium. Solutions were made free from nickel by first passing solutions through a nickel-specific chelation resin. Leaf tip necrosis was observed coincident with the commencement of flowering. (Photograph by David Eskew.) (For a color presentation of this figure, see the accompanying compact disc.)

figure 14.2 Leaf tip necrosis in soybean plants (Glycine max Merr.) grown in nutrient solution provided with equimolar concentrations of nitrate and ammonium. Solutions were made free from nickel by first passing solutions through a nickel-specific chelation resin. Leaf tip necrosis was observed coincident with the commencement of flowering. (Photograph by David Eskew.) (For a color presentation of this figure, see the accompanying compact disc.)

monocotyledons, mottling in dicotyledons) or zinc deficiency (chlorosis and restricted leaf expansion) (1,2,43). Severe toxicity results in complete foliar chlorosis with necrosis advancing in from the leaf margins, followed by plant death.

In pecan growing in the southeastern United States, the long-described but poorly understood symptoms of 'mouse-ear' or 'little-leaf disorder' (Figure 14.4) have recently been shown to be due

figure 14.3 Nickel deficiency symptoms in barley (Hordeum vulgare L. cv. Onda) following 50 days growth in nutrient solution containing equimolar concentrations of nitrate and ammonium. Symptoms include leaf-tip chlorosis and necrosis, development of thin 'rat-tail' leaves, and interveinal chlorosis of young leaves. (Photograph by Patrick Brown.) (For a color presentation of this figure, see the accompanying compact disc.)

figure 14.3 Nickel deficiency symptoms in barley (Hordeum vulgare L. cv. Onda) following 50 days growth in nutrient solution containing equimolar concentrations of nitrate and ammonium. Symptoms include leaf-tip chlorosis and necrosis, development of thin 'rat-tail' leaves, and interveinal chlorosis of young leaves. (Photograph by Patrick Brown.) (For a color presentation of this figure, see the accompanying compact disc.)

figure 14.4 Branches of nickel-sufficient (left) and nickel-deficient (right) pecan (Carya illinoinensis K. Koch). Symptoms include delayed and decreased leaf expansion, poor bud break, leaf bronzing and chlorosis, rosetting, and leaf tip necrosis. (Photo courtesy of Bruce Wood.) (For a color presentation of this figure, see the accompanying compact disc.)

figure 14.4 Branches of nickel-sufficient (left) and nickel-deficient (right) pecan (Carya illinoinensis K. Koch). Symptoms include delayed and decreased leaf expansion, poor bud break, leaf bronzing and chlorosis, rosetting, and leaf tip necrosis. (Photo courtesy of Bruce Wood.) (For a color presentation of this figure, see the accompanying compact disc.)

to nickel deficiency that can be cured by application of nickel (at 100 mg L1) (2). Nickel deficiency in pecan and in certain other woody perennial crops (e.g., plum, peach and pyracantha, and citrus) is characterized by early-season leaf chlorosis, dwarfing of foliage, blunting of leaf or leaflet tips, necrosis of leaf or leaflet tips, curled leaf or leaflet margins, dwarfed internodes, distorted bud shape, brittle shoots, cold-injurylike death of over-wintering shoots, diminished root system with dead fibrous roots, failure of foliar lamina to develop, rosetting and loss of apical dominance, dwarfed trees, and tree death (Wood et al. (2))

Nickel deficiency was long unrecognized in this region because of its similarity to zinc deficiency and as a consequence of a complex set of factors that influences its occurrence. Nickel deficiency is induced by: (a) excessively high soil zinc, copper, manganese, iron, calcium, or magnesium; (b) root damage by root-knot nematodes; or (c) dry or cool soils at the time of bud break (2). The conditions under which Ni deficiency occurs also commonly result in a deficiency of zinc or copper, and this fact has resulted in the extensive use of copper and zinc fertilizers over many years further exacerbating the nickel deficiency. In many horticultural tree species, heavy application of fertilizers with zinc, copper, or both nutrients is common for their nutritional values and benefits for leaf removal and disease protection. In many orchard crops recalcitrant physiological disorders and poorly understood replant 'diseases' are frequent suggesting that induced nickel deficiency may be much more widespread than was previously recognized.

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