Nickel: The last of the essential micronutrients

Abstract

p class="MsoNormal" style="text-align: justify; line-height: normal; margin: 0cm 0cm 0pt; mso-layout-grid-align: none;"> The knowledge about the role of Ni (Ni) in the nutrition, physiology and metabolism of the majority of crops is limited, whereas is considered to be an essential element for the higher plants starting from the 80’s of the twentieth century. The primary function of Ni in plants is defined in terms of its importance for the hydrolysis of urea; however, Ni may have an importance in other physiological processes, such as nitrogen fixation. Although the deficiencies of Ni in plants are relatively rare events, the positive response of yield and nitrogen use efficiency to applications of Ni are shown for different species. The present work summarizes the data about the essentiality of Ni and its function in plant metabolism as well as its agronomic importance for the crops. </p

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Received for publicat ion: 1 December, 2010. Accepted for publication: 2 Febr uary, 2011.
1 Universidad de Ciencias Aplicadas y Ambientales –U.D.C.A. Bogota (Colombia).
2 Department of Agronomy, Agronomy Faculty, Universidad Nacional de Colombia. Bogota (Colombia).
3 Corresponding author: milopez@udca.edu.co.
Agronomía Colombiana 29(1), 49-56, 2011
Nickel: The last of the essential micronutrients
Níquel: el último de los micronutrientes esenciales
Miguel Ángel López1,3 and Stanislav Magnitskiy2
ABSTRACT RESUMEN
e knowledge about the role of Ni (Ni) in the nutrition,
physiology and metabolism of the majority of crops is lim-
ited, whereas is considered to be an essential element for the
higher plants starting from the 80’s of the twentieth century.
e primary function of Ni in plants is dened in terms of its
importa nce for the hydrolysis of urea; however, Ni may have an
importance in other physiological processes, such as nitrogen
xation. A lthough the deciencies of Ni in pla nts are relatively
rare events, the positive response of yield and nitrogen use ef-
ciency to applicat ions of Ni are shown for dierent species. e
present work summarizes the data about the essentiality of Ni
and its function in plant metabolism as well as its agronomic
importance for the crops.
El conocimiento sobre el rol del níquel (Ni) en la nutrición, -
siología y metabol ismo de la mayoría de los cultivos es li mitado;
no obstante, desde los años 80 del sig lo  este elemento se con-
sidera esencia l para las plantas superiores. La función principal
del Ni en las plantas se dene en términos de su importancia
para la hidrólisis de urea, aunque también interviene en otros
procesos siológicos como la jación de nitrógeno. Si bien las
deciencias de Ni en las plantas cultivadas son relativamente
escasas, las aplicaciones de este micronutriente presentan,
en diversas especies, respuestas positivas en el rendimiento
y la eciencia del uso de nitrógeno. El presente trabajo revisa
la esencialidad del Ni y su función en el metabolismo de las
plantas, así como su importa ncia agronómica para los cu ltivos.
Key words: mineral nutrition, essential element, mineral
deciencies, nitrogen cycle.
Palabras clave: nutrición mineral, elemento esencia l, deciencias
minerales, ciclo del nitrógeno.
Introduction
Knowledge about the role of Ni in nutrition, physiology and
metabolism of most crops is currently limited (Bai et al.,
2006). However, the evidence of essentiality of this element
for higher plants is not a new issue, but still goes back to the
70’s of the twentieth century, when a group of researchers
suggested the possible role of Ni in the metabolism of nitro-
gen through its participation in the structure of the enzy me
urease (Dixon et al., 1975). Already in the 80’s Eskew et al.
(1984a), through studies of soybeans, demonstrated the
essential role of Ni in nitrogen metabolism of leguminous
plants, a role that was independent of the form of available
nitrogen (NO3– or NH4+). e evidence generated by this
research suggested the essentiality of Ni for higher plants
(Eskew et al., 198 4b).
e lack of evidence for the role of Ni in non-leguminous
plants was caused by the fact that at that time the studies
about the essentiality were incomplete and, therefore, its
essentiality was not accepted. is gap of knowledge was
supplied by Brown et al. (1987) who established the essential
role of Ni in non-leguminous plants, specically in barley.
ese results together with those obtained previously by
Eskew et al. (1984a) led Brown et al. (1987) to propose a
more support towards the addition of Ni to the group of
micronutrients. Although these studies were, possibly, the
most signicant ones in determining the essentiality of Ni,
there also stood out the studies forwarded by Roach and
Barclay (1946) in plants of potato (Solanum tuberosum),
wheat (Triticum aestivum) and bean (Phaseolus vulgaris)
in England that indicated an increase in plant production
as a result of foliar application of Ni. Additionally, Cataldo
et al. (1978) studied the dynamics and transport of Ni in
soybean plants, while Eskew et al. (1983) founded toxic
levels of urea in the tips of soybean leaves poor in Ni, a
behavior similar to that reported by Walker et al. (1985)
in plant Vignia unguiculata.
e previous studies allowed including Ni within the
group of essential mineral nutrients (Marschner, 2002;
Taiz and Zeiger, 2004; Epstein and Bloom, 2005; Azcon-

50 Agron. Colomb. 29(1) 2011
Bieto and Talón, 2008) and, therefore, it is understood that
plants may not complete the life cycle in the absence of
this nutrient (Arnon and Stout, 1939). Recently, the De-
partment of Agriculture of the USA and the Association
of American Plant Food Control Ocials included Ni as
an essential element for plants, making it possible in the
USA the manufacture and sale of fertilizers containing
Ni (Bai et al., 2006).
Due to the fact that this mineral element is a new one in
the list of essential micronutrients, the objectives of the
present review were to illustrate the current state of re-
search on functions of Ni in plants, in particular, describe
the dynamics of Ni in non-accumulator and accumulator
species, clarify the physiological functions of Ni in plants
as well as symptoms of deciency and toxicity caused by Ni
in plants and identify plant responses to the applications.
Dynamics of nickel in soils and plants
At level of dynamics in soil, Ni is abundant metal in the
earth crust with about 3% of the composition of the earth.
In agricultural soils, typical contents of this element vary
from 3 to 1,000 mg kg-1, however, the soils derived from
basic igneous rocks can contain from 2,000 to 6,000 mg
kg-1 of Ni. Soil pH plays an important role in the avai lability
of Ni, and at pH > 6.7 Ni exists in form of poorly soluble
hydroxides, while at pH < 6.5 increases the presence of
relatively soluble compounds (Brown, 2006).
It is considered that the system of Ni+2 uptake by roots is
similar to that of Cu2+ and Zn2+, a conclusion obtained
aer conrmation of competitive inhibition in absorption
of these three nutrients. When the available concentration
of Ni+2 in the substrate is low (0.5 - 30 mkM), the process
of its absorption by roots is dependent on the expenditure
of ATP, a characteristic that indicates the presence of an
active transport of high anity (Brown, 2006).
Once Ni is absorbed by the root, its movement to the
aboveground parts of plants is closely linked to the for-
mation of organic complexes (Cataldo et al., 1978, 1988;
Bhatia et al., 2005). In general, potential ligands of metals
in plants could be grouped into three classes: oxygen donor
ligands (carboxylates: malate, citrate, malonate, succinate,
and oxalate), sulfur donor ligands (metallothioneins and
phytochelatins), and nitrogen donor ligands (amino ac-
ids) (Baker et al., 2000). In the case of Ni (Ni+2), there was
reported complex formation for its transport in the xylem
with amino acids histidine (Krämer et al., 1996; Brown,
2006) and nicotinamine (Mari et al., 2006) and organic
acids citrate, malate, and malonate (Cataldo et al., 1988;
Robinson et al., 2003; Bhatia et al., 2005), although in the
case of complex with nicotinamine, this one was reported
for the species tolerant or accumulators of Ni (Mari et al.,
2006). At the same time, Homer et al. (1995) suggested that
formation of complexes of Ni in the xylem with molecules
of high molecular weight, such as metallothioneins and
phytochelatins, is an unlikely process.
Complex formation is dependent on pH, such as at low pH
the organic acids are better chelating agents for Ni than
amino acids, whereas at high pH amino acids increase
their capacity to act as ligands (Bhatia et al., 2005). Brown
(2006) indicates that at pH below 6.5 histidine is the most
signicant ligand for Ni, while at pH < 5 citrate is the most
important chelating agent. In oak Quercus ilex, Araujo
et al. (2009) evaluated the eect of four dierent ligands
(histidine, oxalic acid, aspartic and citric acids) present in
the xylem sap on the movement of Ni+2 in the xylem. e
order of anity of ligands towards Ni+2 reported in this
research was: oxalic acid > citric acid > histidine > aspartic
acid. In contrast, the amount of Ni bound to the walls of
the xylem was higher when Ni was present as free cation,
followed by Ni-aspartic acid, Ni-histidine, Ni-citric acid,
and Ni-oxalic acid (Araujo et al., 2009).
Addition of chelating agents to soils with high contents
of Ni may be an eective practice to increase the metal
concentration in soil solution, but have a low eect on in-
creasing of Ni absorption by plants, as showed the study of
Molas and Baran (2004) in barley. is research evaluated
several Ni containing compounds: Ni-citrate, Ni-glutamate,
Ni-EDTA and NiSO4·7H2O and found that the rate of ab-
sorption of Ni by plants arranged from highest to lowest
as NiSO4·7H2O > Ni-citrate > Ni-glutamate > Ni-EDTA.
In Ni non-accumulating species, aer being absorbed and
transported, is used to ensure the functioning of urease,
and, thus, to ensure the hydrolysis of urea to produce
ammonia and carbon dioxide (Marschner, 2002; Taiz
and Zeiger, 2004). Ni in the phloem may be retraslocated
rapidly from the leaves to young tissues, especially during
reproductive growth (Ti n, 1971); this movement is associ-
ated with the formation of complexes with organic acids
and amino acids (Brown, 2006). us, Ni is considered an
element mobile in the phloem (Cataldo et al., 1978; Page
and Feller, 2005), whose mobility is higher than that of
cobalt (Zeller and Feller, 1999). In soybeans, over 70% Ni
present in the leaves could be retranslocated to the seeds
and accumulated mainly in the cotyledons (Tin, 1971;
Cataldo et al., 1978).

51López and Magnitskiy: Nickel: The last of the essential micronutrients
Nickel hyperaccumulator plants
Ni hyperaccumulator species (metallophytes), such as
Stackhousia tryonii, Hybanthus oribundus, laspi caer-
ulescens, Halimione portulacoide, Berkheya coddii, Brassica
juncea, and Typha latifolia are known to accumulate high
concentrations of Ni, among 0.1 and 3.0%, in shoots and
leaves (Ye et al., 1997; Robinson et al., 2003; Bidwell et al.,
2004; Bhatia et al., 2005; Duarte et al., 2006; Mari et al.,
2006; Hsiao et al., 2007). e latex of Sebertia acuminata
(Sapotaceae), a tree native to New Zealand, contains 25.74%
dry weight Ni (Sagner et al., 1998) as well as other cases of
exceptionally high accumulation of Ni in the aboveground
parts of plants are reported; the explanations for Ni hyper-
accumulation are related to the defense role played by high
concentrations of Ni in plant tissues against herbivores and
pathogens (Baker et al., 2000).
It is known that the members of ZIP protein families
(Zinc Regulated Transporters / Iron Regulated Transport-
ers), NRAMP (Natural Resistance Associated Macrophage
Protein), and YSL (Yellow Stripe Like) are involved in the
transport of Ni in dierent organisms. e transforma-
tion of yeasts with ZNT1 or ZNT2 partially conferred Ni
tolerance correlated with the input of Zn, which inhibits
the absorption of Ni. In contrast, transformation with
NRAMP4 conferred sensitivity to Ni in yeasts explained
by a release of Ni from the vacuole (Tejada-Jiménez et al.,
2009). In transgenic plants of Arabidopsis sp., the over-
expression of gene AtIREG2 causes increased tolerance
to high concentrations of Ni. us, it appears that the
physiological function of AtIREG2 may be accumulation
of excess of Ni accompanied by a counter ion (nitrate or
sulphate) in the vacuole to maintain the ionic balance of
cells (Schaaf et al., 2006).
Pianelli et al. (2005) suggested that, in response to elevated
contents of Ni, nicotinamine is translocated from the leaves
of hyperaccumulators to the roots, where it forms com-
plexes with Ni and facilitates its transport to the shoot. In
Arabidopsis sp., overexpression of nicotinamine synthase
confers tolerance to Ni. In addition, the tolerance of plants
to Ni also results from the chelating of Ni in the root with
histidine or organic acids, such as citrate (Tejada-Jiménez
et al., 2009).
Ni hyperaccumulator plants dier from non-accumulators
with the route of transport of this element in the root cor-
tex. e absorption of Ni via the apoplast of the roots of
corn, a non-accumulating plant, ranged from 81.3 to 88.0%,
while that of Leptoplax emarginata, a hyperaccumulator of
Ni, was from 90.6 to 95.5% (Redjala et al., 2010). e root
cell wall in both species had similar anity for the Ni but,
in hyperaccumulator plants, more Ni was absorbed via
the apoplast. is suggests, according to the authors, that
symplastic absorption is not the main factor associated
with hyperaccumulation, and the transport system of Ni
can not be similar in these two species (Redjala et al., 2010).
In hyperaccumulator species, aer absorption and trans-
port via xylem, Ni can be accumulated in vacuoles of leaf
epidermal cells (Krämer et al., 1996; Küpper et al., 2001;
Bidwell et al., 2004; Schaaf et al., 2006), in the cuticle of the
upper epidermis (Robinson et al., 2003) or remain in the
apoplast occupying certain sites in the cell wall (Krämer
et al., 1996; Bidwell et al., 2004). e accumulation of Ni
in the vacuole of epidermal cells is related to the decrease
in the concentrations of K+ and Na+ (Bidwell et al., 2004)
as a likely consequence of a competitive eect between
these cations.
Montargés-Pelletier et al. (2008) reported the carboxylic
acids (citric and malic) as the main responsible agents for
the transfer of Ni in hyperaccumulator plants Alyssum
murale and Leptoplax emarginata. In their research, citrate
was the main ligand of Ni found in stems, whereas in leaves
this function corresponded to malate. Histidine was not
detected in leaves, stems, and roots of plants under study.
In contrast, McNear et al. (2010) founded that, in Alyssum
murale, Ni was in the sap of xylem in a greater proportion
together with histidine, followed by malate and other low
molecular weight molecules. e authors based on their
results adapt a model, in which Ni is transported from
roots to leaves in complexes with histidine and then stored
in the epidermis of leaves and stem in complexes with
malate, other organic acids of low molecular weight and
counter-ions, such as sulfate SO42- (McNear et al., 2010).
Nickel functions in plants: hydrolysis of urea
Ni is chemically related to iron (Fe) and cobalt (Co).
Oxidation state of Ni in biological systems is Ni+2, but it
could also exist as Ni+ and Ni+3 (Marschner, 2002). Ni is a
functional constituent of seven enzymes, six of which are
present in bacteria and animals, while only one, urease
(urea amidohydrolase, EC 3.5.1.5), occurs in plants (Brown,
2006). Constituent participation of Ni in the structure of
urease was rst documented by Dixon et al. (1975) aer its
isolation and description from Canavalia ensiformis. Of the
seven Ni-dependent enzymes two have non-redox func-
tions (urease and glyoxylase) and the remaining ve are
involved in oxidation-reduction reactions (Ni-superoxide

52 Agron. Colomb. 29(1) 2011
dismutase, methyl coenzyme M reductase, carbon mon-
oxide dehydrogenase, acetyl coenzyme A synthase and
hydrogenase) (Brown, 2006).
Metalloenzyme urease is a ubiquitous (everywhere pres-
ent) (Malavolta and Moraes, 2007) enzyme that consists
of six identical spherical subunits, each with two atoms of
Ni (Dixon et al., 1980; Hirai et al., 1993) whose molecular
mass is reported in the range of 473-590 kDa (Fishbein
et al., 1973; Dixon et al., 1980). Within the subunits, the
union of Ni is coordinated by ligands containing N- and
O- (Marschner, 2002).
Although it is considered that Ni is not required for the
synthesis of urease, this element is an essential metal
component in the structure and catalytic function of the
enzyme (Hirai et al., 1993; Marschner, 2002). In soybean
urease, its synthesis is directed by a long chain of RNA
consisting of 3,000 to 3,500 nucleotides and their partici-
pation on the total weight of extractable seed protein is of
the order of 0.2% (Polacco and Sparks, 1982).
e role of urease is to catalyze the hydrolysis of urea
CO(NH2)2 to ammonia (NH3) and carbon dioxide (CO2),
a reaction that occurs mainly in leaves (Marschner, 2002;
Taiz and Zeiger, 2004; Malavolta and Moraes, 2007; Azcon-
Bieto and Talón, 2008). e above statement may indicate
that the functionality of Ni is restricted to those crops,
where nitrogen inputs are derived from urea, however,
this assumption is not correct; the essentiality of Ni is
due to the formation of urea interior of plants as a result
of metabolic pathways common to all plants that include
the catabolism of purines (adenine and guanine), ureides
and protein catabolism of arginine via ornithine cycle and
conversion of canavanine to canaline in certain plants
(Wa lker et al., 1985).
Other functions of nickel in plants
Ni is also involved in symbiotic nitrogen xation through
its role as an active center of hydrogenase, a process
documented in strains of nitrogen-xing bacteria Brady-
rhizobium japonicum, Bradyrhizobium sp. (Lupinus sp.),
Rhizobium tropici, Rhizobium leguminosarum, and Azo-
rhizobium caulinodans (Palacios, 1995). Hydrogenase is an
enzyme responsible for oxidizing the hydrogen produced
by nitrogenase during symbiotic nitrogen xation result-
ing in the production of ATP and, therefore, this enzyme
increases the eciency of symbiotic process, and decreases
the inhibitory activity of hydrogen in the bacteroids (Pala-
cios, 1995; Ruíz-Argueso et al., 2000). us, the low level
of Ni in agricultural soils may limit the activity of hydrog-
enase from R. leguminosarum and, therefore, the eciency
of symbiotic nitrogen xation in legumes (Ruiz-Argueso
et al., 2000; Malavolta and Moraes, 2007).
Zobiole et al. (2010) in Brazil showed that application of
glyphosate can negatively inuence symbiotic nitrogen
xation in soybeans grown in soils with low native con-
centrations of Ni in response to a decrease in the foliar
concentration of this element. In Matricaria chamomilla,
accumulation of chlorogenic acid, an important antioxi-
dant compound, was increased almost fourfold in response
to the application of 120 mkM Ni to the substrate (sand).
It is, therefore, proposed that Ni may have antioxidant
properties of phenolic metabolites (Kovacik et al., 2009).
Being similar to cation of iron, cation of Ni may have bene-
cial functions for the formation of anthocyanins that con-
tain iron or aluminum as structural elements. According
to Aziz et al. (2007), applications of Ni to soil contributed
to accumulation of anthocyanins and avones in plants of
Hibiscus sabdaria when applying 20-25 mg kg-1 Ni.
Deficiencies and toxicities of nickel in plants
Ni deciency in legumes and other dicots causes a decrease
in the activity of enzyme urease, a condition that causes
accumulation of toxic levels of urea and is manifested as
necrosis at the tip of the leaves (Eskew et al., 1983; Walker
et al., 1985; Malavolta and Moraes, 2007). In soybean,
low levels of Ni in soil reduced nodulation (Zobiole et al.,
2010) and seed yield, a phenomenon that is explained by
the involvement of Ni in hydrogenase activity of bacteroids
(Brown, 2006). At the same time, due to the relatively low
requirements of plants in Ni, the events of Ni deciencies
in the eld are few, while the toxicities caused by Ni are
more common (Mengel and Kirkby, 2001).
Decreased urease activity in non-timber species can in-
duce the deciency of nitrogen and aect the contents of
amino acid amides (asparagine and glutamine) and inter-
mediates of urea cycle (arginine, ornithine, and citrulline)
(Bai et al., 2006). In grasses, on the other hand, deciency
symptoms include intervenal chlorosis and necrotic spots
on young leaves. In general, urea accumulation in the tip
of the leaves (necrosis) of both monocotyledonous and
dicotyledonous plants is diagnostically symptom of Ni
deciency (Brown, 2006).
One of the best documented cases of the deciency of Ni
is the perennial timber pecan Carya illinoinensis. In this

53López and Magnitskiy: Nickel: The last of the essential micronutrients
species, Ni deciency is known as “mouse ear” or “little
leaf disorder” (Malavolta and Moraes, 2005; Bai et al., 2006)
and was rst proved as a deciency of Ni in 2004 by Wood
and colleagues (Malavolta and Moraes, 2007). However, the
symptom is reported in the United States since 1918 and is
characterized by the presence of round dark spots on t he tips
of new leaves and curving of leaf blade to make the appear-
ance of the ear of a mouse (Malavolta and Moraes, 2005).
In pecan, Ni deciency aects nitrogen metabolism via
ureide catabolism, amino acid metabolism and ornithine
cycle intermediates and metabolism of carbon through the
accumulation of lactic acid and oxalic acids that accumu-
late on the edges of leaf blade and would also be linked to
necrosis of the tips of the leaves (Bai et al., 2006).
Ni deciency in pecan could be corrected by foliar applica-
tion of Ni; however, the dose of Ni reported in the literature
is variable. us, Brown (2006) indicates that a dose of Ni
equal to 100 mg L-1 is sucient to correct the deciency,
while Malavolta and Moraes (2005) recommended spraying
a solution of 0.8 g L-1 Ni mixed with a dose of 4.8 g L-1 urea.
Malavolta and Moraes (2005) and Brown (2006) indi-
cated that the main factors that favor the development
of Ni deficiency are: a) excess of Cu and Zn that com-
petitively inhibits the absorption of Ni by roots, b) soil
pH > 6.5 (formation of low soluble hydroxides and Ni
oxides), c) soils with high contents of Fe, Mn, Ca, or Mg,
d) excessive doses of nitrogen or excessive liming, e)
high levels of soil phosphorus that favor the formation
of phosphates of Ni and decrease the absorption of Ni by
plants; f) inhibition of urease activity by accumulation
of Cu in plants.
In soils developed over ultrabasic rocks, high levels of Ni,
such as exceeding 250 mg kg-1 soil, may lead to Ni toxicity
in non-accumulator plants (Mengel and Kirkby, 2001).
e symptoms of Ni toxicity may resemble the symptoms
of iron deciency due to a reduced absorption of iron in
soils high in Ni (Mengel and Kirkby, 2001). e critical level
of Ni in leaves varies according to species, but generally a
suitable range is considered between 1 and 10 mg kg-1 dry
matter basis (Marschner, 2002), higher than 25 mg kg-1 lead
to Ni toxicity in non-accumulator species (Malavolta and
Moraes, 2007) through distortions in the growth of root
system and leaf buds (Brown, 2006). In wheat, the addition
of 50 and 100 mkM Ni to the growth substrate resulted
in decrease of fresh weight of shoot, the nitrate content, a
reduction in the activity of nitrate and nitrite reductase,
40 and 80% less, respectively (Gajewska and Skłodowska,
2009). In contrast, an increase in ammonium content, pro-
line concentration, and the activity of NADH-glutamate
synthase in plants treated with toxic levels of Ni was re-
ported (Gajewska and Skłodowska, 2009). e toxicity of
Ni in plants may be alleviated by liming or application of
phosphate fertilizers that reduce availability of Ni to the
plants (Mengel and Kirkby, 2001).
Plant yield response to applications of nickel
e response of plants to applications of Ni is wide and
includes eects on nitrogen xation, seed germination and
disease suppression. However, a much higher eect could
be seen when nitrogen is provided in the form of urea or
symbiotically xed (Brown, 2006).
e rst evidence of the y ield response to Ni was document-
ed by Roach and Barclay (1946), who reported a signicant
increase in crop yields of potato (Solanum tuberosum),
wheat (Triticum aestivum) and bean (Phaseolus vulgaris)
as a result of foliar application of Ni from dilute solutions.
In soybean, it was found that the addition of 40 g ha-1
Ni increases nodulation and crop yield (Malavolta and
Moraes, 2007), an eect attributed to the proper function-
ing of the symbiosis between soybean and Rhizobium sp.
(Brown, 2006). In parsley (Petroselinum crispum) growing
in plastic containers with clay, the addition of 50 mg kg-1
soil Ni from NiSO4 source increases the yield and qual-
ity of leaves, reduces the accumulation of NO3- and NH4+
and increases the accumulation of essential oil aroma
constituents (Atta-Aly, 1999). On the other hand, in Brazil
the application of 0.03 mg L-1 Ni in nutrient solution of
umbu seedlings (Spondias tuberosa) increased dry mass
production by 81.52% compared to untreated control
(Caires et al., 2007).
In rose of Jamaica (Hibiscus sabdaria), Aziz et al. (2007)
found that a joint application of cobalt and Ni in doses of
20 and 25 mg kg-1 soil, respectively, increases the total mass
of the plants, branch number and dry weight and fresh
weight of owers. In addition, these applications promoted
an increase in the concentration of N, P, K, Co, Ni, Mn,
Zn, and Cu, both in leaves and owers of the plants (Aziz
et al., 2007).
Gad et al. (2007) in tomato (Lycopersicon esculentum)
grown in sand found that the addition of 30 mg kg-1 sand
Ni signicantly increased the total mass of the plant,

54 Agron. Colomb. 29(1) 2011
number of branches, leaf area, root length, contents of
auxins and gibberellins. Similarly, the addition of Ni in
the aforementioned doses improved fruit quality variables
such as size, fresh weight, diameter, dry weight, contents
of vitamin C, total soluble solids, and soluble sugars. In
addition, the application of Ni caused the decrease in the
contents of NO3- and NH4- as well as acidity, favorable
characteristics for consumer health (Gad et al., 2007).
Finally, it has been shown a benecial eect of Ni in the
management of agents causing fungal diseases, such as
rust of cereal crops (Brown, 2006; Malavolta and Moraes,
2007). e benecial eect is attributed to the alleged role
of this element in reactions involving enzymes, such as
superoxide dismutase, changes in nitrogen metabolism
due to the contribution of Ni (Brown, 2006) and the
possible toxicity of Ni to the pathogen (Malavolta and
Moraes, 2007).
Changes in nitrogen metabolism may involve the decrease
in amount of free amino acids, a substrate used by most
pathogens for growth and proliferation (Strengbom et
al., 2002). e accumulation of free amino acids, such
as valine, leucine, isoleucine, tyrosine, tryptophan, and
arginine, in response to Ni deciency was reported by
Bai et al. (2006). In practical terms, the eciency of foliar
sprays of urea in dierent crops can be improved by their
joint application with Ni (NiSO4) at levels not exceeding
40 g ha-1 of Ni for crop cycle.
e application of Ni may have positive eects on nitrogen
use eciency in crops that extract high content of this
mineral nutrient from soil and where nitrogen fertilizers
are applied using urea as the main source, such as in case
of rice. However, such eects could only be veried by
conducting a research involving Ni as a case study.
Conclusions
e current state of research dedicated to physiology of Ni
in plants illustrates the essentiality of this micronutrient for
plants, in par ticular, its importance for the processes related
to the metabolism of nitrogen. e primary function of Ni
is dened in terms of its importance for the hydrolisis of
urea; however Ni may have an importance in other physi-
ological processes, such as nitrogen xation and synthesis
of anthocyanins. Although the deciencies of Ni in plants
are relatively rare events, the positive response of crop yield
and nitrogen use eciency to applications of Ni are shown
for dierent species.
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