African Journal of Biotechnology Vol.11(46), pp.

10462-10468, 7 June 2012

Available online at http://www.academicjournals.org/AJB
DOI:10.5897/AJB12.477
ISSN 1684-5315 ©2012 Academic Journals

Review

Foliar nutrition in apple production

Senad Murtic1*, Hamdija Civic2, Milena Ðuric3, Gordana Šekularac4, Radisav Kojovic5,
Mirko Kulina6 and Milorad Krsmanovic 5
1
Department of Botany and Plant Physiology, Faculty of Agriculture and Food Sciences, University of Sarajevo,
Bosnia and Herzegovina
2
Department of Plant Nutrition, Faculty of Agriculture and Food Sciences, University of Sarajevo,
Bosnia and Herzegovina
3
Department of Plant Physiology, University of Kragujevac, Faculty of Agriculture Cacak, Serbia
4
Department of Water Menagement, University of Kragujevac, Faculty of Agriculture Cacak, Serbia
5
Faculty of Agriculture Cacak, University of Kragujevac, Serbia
6
Faculty of Agriculture, University of East Sarajevo, Republic of Srpska, Bosnia and Herzegovina
Accepted 25 May, 2012

In order to create conditions conducive to sustainable fruit production, involving optimum utilization of
all sources of plant nutrients with minimum environmental pollution, it is necessary to reorient
agricultural producers to use those types of fertilization that are environmentally safe and appropriate
which can also satisfy all fruit tree nutrient requirements. This gives particular importance to foliar
nutrition as this model poses the lowest risk of soil and groundwater contamination with undesirable
mineral elements. The objective of this study was to provide a comprehensive review of research
papers dealing with the effect of foliar feeding on development parameters in apple trees in an attempt
to obtain a more thorough insight into the advantages and disadvantages of this fertilization type and
facilitate the potential use of this practice for apple producers.

Key words: Malus x domestica, foliar fertilization, nutrient, leaves.

INTRODUCTION

Successful fertilization in the cultivation of apples and adversely affect soil and crop quality (Khan et al., 2005;
fruit crops in general requires not only definition of Abdelaziz et al., 2007).
fertilizer application rates but also adequate use of A large part of the nutrients applied remain unused by
suitable fertilization types. The fertilization type used can the fruit tree and leach into deeper soil layers, causing
substantially alter and disturb the growth and soil and groundwater contamination. Groundwater
development of a fruit tree if fertilizers are applied contamination ranks among the most serious problems
incorrectly, regardless of the adequately predefined fruit facing the world today since it entails risks for the supply
tree nutrient requirements (Hanić et al., 2009). Different of drinking water in the future, also leading to other
types of fertilization are used in fruit production, including environmental degradation problems such as disturbance
fertilization with mineral fertilizers (conventional type), of biological processes and prevention of the normal
fertigation, foliar nutrition and a range of other types. In development of the flora and fauna of aquatic systems
order to achieve high yields and ensure simplicity of use, (Kang et al., 2008). Due to the aforementioned reasons,
some producers use only conventional types of in the cultivation of apples and other fruit crops, scientists
fertilization. These nutrition types, characterized by give priority to fertigation and foliar nutrition, as well as
excessive use of mineral fertilizers and chemicals, and types that significantly improved the efficiency of
very often by injudicious fertilizer applications at plant fertilizers, with minimum adverse environmental impact
phenostages, lead to increased yields, but indirectly (Zydlik and Pacholak, 1998; Naseri et al., 2002; Amiri et
al., 2008).
Although fertigation is generally seen as a preferred
type of fertilization, foliar nutrition has been used very
*Corresponding author. E-mail: [email protected]. often lately in fruit production. The main advantage of
 Murtic et al. 10463

Figure 1. Structure of plant cuticle.

foliar nutrition is that it can be used under very limited 1965; Schonherr and Huber, 1977; Franke, 1986).
root nutrient uptake conditions (root damage, long The first knowledge of the mechanism of nutrient
periods of dry weather, and stagnation of water on uptake through leaves dates back as early as the second
surface of soil). Furthermore, the degree and rate of half of the 18th century, but this problem was given
th
nutrient utilization through foliar fertilizers are higher than serious scientific attention in the second half of 20
those through soil fertilizers, particularly at low century. The long-held scientific belief was that nutrient
temperatures (Wojcik, 2004; Pfeiffer et al., 2008). uptake though leaves are impossible, mostly due to the
Additionally, this type of fertilization largely contributes to cuticle which was deemed completely impermeable to
environmental protection by reducing undesirable nutrient water and dissolved substances. However, progress in
leaching from the soil, an accompanying manifestation of the fields of chemistry, biochemistry and plant physiology
most other fertilization types (Dong et al., 2005; Totten et has enabled better insight into the leaf anatomical
al., 2008). Using the advantages of foliar feeding in fruit structure and nutrient uptake potentials, leading to the
cultivation requires knowledge of mechanisms of nutrient knowledge that the penetration of substances through the
uptake through leaves as well as of factors governing cuticle and, hence, indirectly, into leaf mesophyll cells, is
nutrient entry into the leaf. Knowledge of these factors possible and highly effective (Franke, 1967).
will enable adequate preparation of foliar fertilizers and The cuticle is the outer layer of leaf epidermal cells.
their use in accordance with plant requirements in certain The diagram in Figure 1 illustrates the basic structure of
phenophases of plant development. the plant cuticle of epidermal cells (Hess, 1991). The
cuticle is composed of a matrix comprising cutin (a
MECHANISM OF NUTRIENT UPTAKE THROUGH polymer of inter-esterified C16 and C18 hydroxyfatty acids)
LEAVES and cuticular wax (composed of long-chain hydrocarbons
C22 to C34, alcohols, fatty acids and esters) and on the
Nutrient uptake through leaves is based on the entry of surface of cuticle has a layer of epicuticular wax (Baker,
dissolved salts mostly through the cuticle and to a much 1982). This composition of the cuticle is a highly lipophilic
lesser extent through the leaf stomata (Kannan, 1980). character, which considerably impedes the entry of
Nutrient entry through the stomata is negligible as the nutrients that is, dissolved ions through the cuticle.
openings are small, occupy little space, and their opening However, when hydrated, the cuticle becomes swollen,
reduces due to leaf wetting (Zeiger, 1983). The entry of causing ectodesmata, that is, pores or spaces between
nutrients through the cuticle is also hampered since the the molecules which build cutin to increase, creating the
cuticle, due to its structure, acts as a barrier to nutrient pathway for ions to pass through (Schnönherr, 2006).
uptake. Nevertheless, some nutrients can pass through The older and thicker the cuticle, the lower the hydration
the cuticle, depending on the structure, chemical ability; hence, the cuticle permeability (Bargel et al.,
composition, age, thickness and hydration status of the 2006). Since the cuticle on the underside of the leaf is
cuticle, as well as on nutrient properties (Yamada et al., somewhat poorly developed, it is particularly important to
10464 Afr. J. Biotechnol.

treat this very part of the leaf for increased effect of foliar completely spans the plasma membrane. Also, channel
fertilizers (Abbott et al., 1990). Once they pass through protein can either be aqueous channels or ion channels.
the cuticle, the next obstacle the dissolved ions come Aqueous channels are always open, showing poor
across is part of the cell wall composed of cutin, hemi- selectivity and transporting most of the water and
cellulose and, to a large part, of pectin. dissolved substances. Ion channels are highly selective,
Pectin is a polymer of galacturonic acid whose being involved solely in ion transport (Amtmann and Blatt,
molecules are negatively charged due to the high 2007). Ion channels have a highly specific structure; they
presence of free carboxyl groups. The difference in are shaped like tubes with the middle part expanded and
charge between pectin and upper layers of epidermal the tube lumen abruptly narrowing towards the surface of
cells results in the creation of an electrochemical gradient membrane into a very tiny openings. These openings
which facilitates the passive transport of cations and which are called ion-selective filters allow only ions
water molecules (Baur et al., 1997). Estimates suggest whose shape and size fit the filter to pass through the
that it is due to this negative charge of pectin that the membrane (Krol and Trebacz, 2000). Importantly, the
ability of cations penetrates through the outer layer of the filters are generally closed, as they open only upon
leaf epidermis which is thousand times that of anions specific stimuli produced by the internal cell metabolism
(Tyree et al., 1990). As regards cations having the same or a particular external stimulus which eventually, through
valence, priority in the absorption process is given to hormones, lead to channel opening.
smaller cations (McFarlane and Berry, 1974). Generally, Calcium, chloride, sodium (Na) and potassium (K) ions
it is suggested that this part of ion movement through are transported mostly through ionic channels (Chen and
these cell wall layers is attributed to both cuticle structure Eisenberg, 1993). Apart from ionic channels, the
and the electrochemical gradient occurring due to charge transport of ions through the plasma membrane is also
differences between particular layers (Tyree et al., 1992). regulated by protein carriers. Protein carriers also span
The next cell wall layer that ions come across is mostly the plasma membrane; they contain molecule- or ion-
made of hydrophilic cellulose molecules and as such it specific binding sites in their interior. Upon adhesion to
does not obstruct the movement of the ions until they the binding sites, the substance travels to the opposite
reach the plasma membrane (Holloway, 1993). end of the carrier protein and then it separated
The plasma membrane is the last obstacle to be (Eisenberg, 2003). Whether passing through ionic
overcome by nutrients, during their passage into the cell's channels or carriers, ions are transported through the
interior. Nutrients are actually up taken by leaves only plasma membrane via the active pathway; from a low
after permeation through the plasma membrane, which is concentration area (foliar fertilizers) to a high
physiologically analogous to root nutrient uptake concentration area (leaf).
mechanisms. The plasma membrane is a thin membrane However, the use of foliar fertilizers containing a high
having a highly organized structure which surrounds the concentration of active ingredients would disturb the
cytoplasm of each cell; it consists of a lipid bilayer that osmotic equilibrium within leaf cells, and that would have
has a fluid consistency with protein molecules embedded negative impact on the functions of plant cells. This
in it on both the outside and inside of the membrane problem is seen as the key deficiency of foliar feeding
(Robertson, 1960). Being largely hydrophobic in because the need for some elements (nitrogen (N),
character, the lipid part of the plasma membrane is an phosphorus (P), K) are considerably higher than their
unsurpassable obstacle to the movement of ions, concentrations that can be placed in the foliar fertilizers
regardless of their size (Mengel, 2002). This suggests without toxic effects on the leaves (Marschner, 1995).
that hydrophilic molecules can move only through the The passage of nutrients through the plasma membrane
protein part of the membrane. As regards the position of is followed by their simple transport from one cell to
proteins in the matrix of the plasma membrane, the another through membranes, as aforementioned, and
hydrophilic ends of the proteins (an amino group and a through plasmodesmata, cytoplasmic strands that
carboxyl group) are always oriented towards the outside connect the protoplasts of adjacent cells (Sanders and
of the surface of membrane, and hydrophobic ends of the Bethke, 2000). This is how all chloroplast-containing
proteins (short-chain carbohydrates) towards the lipid mesophyllic cells are supplied with nutrients vital for
parts of the membrane. This position of the proteins photosynthesis.
facilitates the passage of ions and hydrophilic molecules
in general through the protein part of the plasma
membrane without their coming into contact with the lipid FACTORS GOVERNING NUTRIENT ENTRY INTO THE
parts of the membrane (Maurel, 1997; Burton et al., LEAF
2010).
Proteins involved in ion transport through the plasma Apart from the structure of the cell wall and that of the
membrane can either be channel proteins or carrier plasma membrane, nutrient uptake through the foliage is
proteins (Chrispeels et al., 1999). Channel proteins are also dependent upon the following factors: Rate of
generally built from a single protein molecule that nutrient uptake, nutrient mobility in the plant,
 Murtic et al. 10465

temperature, and morphological and anatomical which is not based on these parameters, in generally has
characteristics of the leaf. The efficiency of nutrient a negative effect on plant development.
uptake through leaves increases with increasing rate of In order to create conditions conducive to sustainable
nutrient uptake and mobility in the plant. Mineral fruit production involving optimum utilization of all sources
elements can be divided into three groups according to of plant nutrients with minimum environmental pollution, it
the rate of their uptake in leaves: high uptake rate (N, K, is necessary to reorient agricultural producers to use
Na, zinc (Zn), and Cl), medium uptake rate (Ca, sulphur types of fertilization that are environmentally safe and
(S), P, manganese (Mn) and boron (B)) and low uptake appropriate. This gives particular importance to foliar
rate [magnesium (Mg), copper (Cu), iron (Fe) and nutrition as this model poses the lowest risk of soil and
molybdenum (Mo)]. For most nutrients (N, K), their groundwater contamination with undesirable mineral
mobility in plant is positively correlated with the uptake elements. This model is being promoted through latest
rate (Bukovac and Wittwer, 1957; Tukey et al., 1962). findings on mechanisms of absorption of foliar fertilizers,
Nutrient uptake is positively affected by increasing as well as through an abundant choice of structurally
temperature until the optimum temperature for nutrient diverse clear solution, suspension and powder fertilizers
uptake is reached, the optimum value depending on the which exhibit exceptional efficiency.
nutrient being up taken (Reed and Tukey, 1982). Most scientists share the belief that the main
When comparing nutrient uptake through the root and advantage of foliar feeding is that it can be used under
that through the leaf, many studies have confirmed higher very limited root nutrient uptake conditions. Hanić et al.
nutrient uptake through the foliage at low temperatures. (2009) highlighted the particular efficiency of foliar
This is especially true of phosphorus which is, at low soil fertilizers in the uptake of ions that show antagonism in
temperature almost solely adopted through the leaf the soil solution or low mobility in the soil. Thalheimer and
(Hurewitz and Janes, 1983). Nutrient uptake is also Paoli (2002) found that magnesium is very difficult to
largely affected by the morphological and anatomical adopt through the root, mostly due to its antagonism with
+
structure of the leaf, primarily cuticle structure. Increasing some elements, notably NH4 ions. The same problem
age and increasing thickness of the cuticle lead to a occurs with the uptake of Ca which is absorbed with
decrease in cuticle swelling capacity and, hence, nutrient difficulty from the soil solution due to its antagonistic
uptake ability. Therefore, it is best to use foliar fertilizers relationship with K as well as with NH4+ and Mg ions
to treat young well-developed leaves, on their underside (Trivedi, 2006). Foliar nutrition which contain Ca and Mg
in particular, due to a thinner cuticle on this side. Nutrient in greater amounts can help avoid these disadvantages
entry into the leaf is also considerably dependent upon while improving certain fruit quality parameters in apples,
nutrient properties: Form of active ingredients, type of their storability in particular (Wojcik and Szwonek, 2002;
dissolved ions, pH, and content and ratio of mineral Lanauskas and Kvikliene, 2006).
nutrients in the solution. The characteristics mentioned Calcium has a very important role in increasing fruit
earlier govern the ability, rate and method of nutrient storability. It is reported that apple fruits have good
uptake from fertilization (Wojcik, 2004). storability if their Ca levels are above 4.5 mg/100 g fresh
fruit (Dris et al., 1998). If the amount of Ca falls below this
value, there is a high risk of damage to the skin, and
DISCUSSION AND PERSPECTIVE OF USE OF consequently internal parts of the fruit. Namely, calcium
FOLIAR FERTILIZERS IN APPLE GROWING is vital for fruit firmness, being involved in the formation of
calcium pectinates and oxalates which provide firmness
Apple trees remain in the same positions for over ten to the outer parts of cell membranes. When the
years regardless of whether the extensive or intensive membranes are weakened, there is an uncontrollable
method of production is used. Soils, even those richest in loss of water which contributes to the decay of the
nutrients, do not contain enough nutrients for regular and surface layer and, consequently, the inner layer of the
abundant yields on a yearly basis. Therefore, apple tissue. Visual manifestations include the occurrence of
growers who are seriously engaged in fruit production dark brown or black bitter pits. Given the damage of the
need to incorporate additional nutrient amounts into the layer, these areas become susceptible to different
soil in order to achieve satisfactory fruit yield and quality. pathogens (Freitas et al., 2010). Bitter pit incidence can
Due to the specific nature of fruit production, climate and be prevented by the supply of sufficient amounts of
edaphic conditions in an orchard, biological properties of calcium to apple fruits (Pooaviah et al., 1998).
apple fruit, and interactive effects of other environmental Rates and forms of calcium fertilizers to be applied
factors, there is simply no single recipe for fertilization. should be defined based on the mechanisms of calcium
However, there is guideline on fertilization rates uptake and movement within the plant. As opposed to
determined based on research findings. These rates are most macronutrients, calcium has low mobility within the
specific, relating only to the investigated site, and are plant. Its mobility is somewhat more pronounced in the
defined based on soil pH, nutrient content in the soil and ascending direction, from the roots up to the leaves,
fruit requirements. Any fertilization recommendation whereas calcium movement in the opposite, from leaves
10466 Afr. J. Biotechnol.

to fruit is limited. When calcium is up taken through the inactivated primarily due to excessive pH. Zinc deficiency
root, during its ascending movement, the already can adversely affect bud formation; therefore, zinc should
absorbed calcium is being diluted, which results in be supplied to the apple tree, the easiest and most
decreased influx of Ca into the fruit. Given both the above efficient method on carbonate soils being foliar treatment
and the potential antagonism of calcium in the soil of fruit trees with zinc in the sulphate (ZnSO4) and
solution with many elements (K, NH4, Mg), it is clearly chelated form (Neilsen and Hogue, 1983).
suggested that calcium nutrition should be carried out The positive effect of foliar feeding on the fruit yield and
foliarly, by direct treatment of fruits with a calcium quality of apple has also been dealt with by other authors
fertilizer containing more readily absorbable forms of (Štampar et al., 1998; Tagliavini et al., 2000). Veberić et
calcium, such as calcium nitrate (Lodze et al., 2008) or al. (2002) associate yield increases induced by foliar
calcium chloride (Shirzadeh et al., 2011). A positive effect applications of phosphorus and potassium with certain
of the combined use of 1% calcium nitrate and 0.5% photosynthetic parameters. Hanić et al. (2009) underline
calcium chloride on the storability of apple fruits has been the favorable use of foliar fertilization in feeding old apple
reported by Moor et al. (2006). orchards where the possibility of receiving mineral
The storability of apple fruits is dependent not only elements from the soil solution decreased due to the
upon calcium levels, but also upon the content of other exhaustion of soil. Although a large number of studies
elements, including primarily phosphorus, potassium, have proven the positive effect of foliar nutrition, if applied
magnesium and nitrogen (Perring, 1968). If phosphorus in accordance with fruit requirements, on fruit yield and
levels in apple fruits are below 9 mg/100 g fruit, there is a quality, foliar nutrition is not recommended as a uniform
great risk of bitter pit occurrence, particularly at a very fertilization type. The largest problem with foliar feeding is
low Ca concentration in apple fruits (Johnson, 1980). The that is not able to completely replace the nutrition through
efficient use of foliar feeding with phosphate fertilizers in the roots, primarily due to plant requirements for some
preventing bitter pit occurrence and increasing fruit elements (N, K, P) is considerably higher than their
quality in general has been reported by many scientists concentrations in the foliar fertilizers. As part of adequate
(Yogaratnam et al., 1981; Wojcik and Wojcik, 2007). The nutrition, fruit trees should be frequently sprayed, which
content of calcium versus phosphorus, a high would however lead to an increase in production costs.
concentration of potassium in apple fruit is not desirable, Although it cannot be used as a uniform model of
or more precisely is not desirable high ratio between fertilization, foliar fertilization can serve as an excellent
content of potassium and calcium in apple fruit. The supplement to other fertilization types (Doring and
storability of apple fruits is considered to substantially Gericke, 1986).
decrease at the potassium to calcium ratio in apple fruits Importantly, in order to ensure success of foliar
of over 30:1 (Winska-Krysiak and Lata, 2010). The high applications, experts in this field should be consulted
concentrations of nitrogen are equally undesirable in before foliar treatment to ensure the unobstructed
apple fruit since they cause increased susceptibility to development of the fruit tree and optimum quality of the
pathogens, a decline in fruit firmness and an overall fruit. Some advice that may be useful in foliar applications
decrease in fruit storability (Blaszczyk and Ben, 1996). It include the following: treatments should not be performed
is noteworthy that the foliar feeding of apple trees with at high temperatures (above 23°C) due to the risk of
macronutrients, including nitrogen, potassium and dehydration of the solution out of the leaf surface, or
phosphorus, is not easily achievable, mostly due to the during windy weather in order to prevent droplet drift and
inability of foliar feeding to satisfy the large fruit demand avoid mistakes in the treatment. Moreover, the leaf
for these elements. underside should preferentially be treated as much as
However, foliar feeding has proven to be an extremely possible due to the considerably thinner cuticle on this
effective method for correcting deficiencies of side. In order to enhance the adhesion of foliar fertilizers
micronutrients in plants, primarily boron and manganese to the leaf, it is advisable to use agents that reduce the
as key biogenic elements in apple fruit development. surface tension between the solution and the cuticle.
Boron plays a very important role at the stage of When mixing two or more foliar fertilizers, special care
pollination, contributing to pollen tube vitality and fruit should be given to the ratio of elements in the fertilizer
development, whereas manganese is an important used so as to avoid adverse effects on nutrient uptake.
micronutrient involved in water photolysis and electron When mixing foliar fertilizers with crop protection agents,
transport in the light-dependent stage of photosynthesis one should avoid copper- and sulfur-based protection
(Nešković et al., 2003). A positive effect of foliar feeding agents and those having a high pH in order to prevent
with B and Mn on development parameters in apples has their adverse effect on growth and development
been obtained by many scientists (El-Shazly, 1999; parameters in apple. If all of the aforementioned facts are
Stover et al., 1999; Naseri et al., 2002). Foliar feeding considered and if foliar treatments are conducted in
has also proven to be highly efficient in the uptake of Zn if accordance with manufacturers' instructions and plant
apples are cultivated on alkaline and carbonate soils requirements during particular phenostages, a positive
where the absorption of Zn from the soil solution is effect on the quality of apple fruits can be expected,
 Murtic et al. 10467

particularly in terms of increasing their storability Franke W (1986). The basis of foliar absorption of fertilizers with special
regard to the mechanisms. In: A. Alexander (ed.), Foliar fertilization.
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