Nanotechnology promotes the R&D of new-generation micronutrient foliar fertilizers

Abstract

Foliar fertilizers have attracted increasing attention over the last few decades as they offer the most efficient way to correct micronutrient deficiencies and enhance the product yield and quality of crops and plants. The micronutrients are essential to physiological functions in plant metabolism, and leaf uptake has been extensively studied as a biological process, however, the mediating factors are still unsolved. This review presents the current efforts of chemical engineers and nanomaterial scientists to solve the problems by taking the advantages of nanotechnology and designing and developing new-generation long-term foliar micronutrient fertilizers. The important physiological functions of the most important micronutrients (zinc, manganese, copper, and iron) have been briefly reviewed to illustrate the significance of the relevant research. Current foliar fertilizers have then been assessed in terms of their solubility, morphology and surface properties. The new screening criteria of new-generation micronutrient foliar fertilizers have been put forward from the viewpoints of material engineers, and our recent research efforts using nanotechnology to design and develop new foliar fertilizers have been summarised. Finally, our opinions for further development of long-term micronutrient foliar fertilizers have been proposed based on the nanotechnology.

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Peng Li

Peng Li acquired his BSc degree from Wuhan University of Technology (Hubei, China) in 2002 and Master degree from Chalmers University of Technology (Sweden) in 2005. After working for Tsinghua Science Park (Zhuhai) for 3 years, Peng was enrolled in Australian Institute for Bioengineering and Nanotechnology, the University of Queensland and awarded PhD degree in 2013, and is currently a postdoctoral research fellow here. His research area is functional nanomaterials with industrial potential and his recent research focuses on synthetic nanoclay or clay-matrix nanocomposites for various agricultural applications.

Longbin Huang

Longbin Huang graduated with his BSc degree from Jiangxi Agricultural University in 1986 and his PhD degree from Murdoch University (Perth, Australia) in 1994. After his PhD, he worked as a postdoctoral/research fellow in Murdoch University. He joined the University of Queensland as a lecturer of plant mineral nutrition in 2004 and was promoted to senior research fellow in 2007 and principal research fellow in 2014. Longbin's research theme is Ecological Engineering of Soil-Plant Systems, including fertiliser technology, soil metal(loid) contamination remediation technology and technology in mine waste rehabilitation.

Neena Mitter

Associate Professor Neena Mitter, at the Queensland Alliance for Agriculture and Food Innovation, the University of Queensland, has been involved in biotechnology research in Australia and India for over 20 years. The group led by her focuses on developing RNA interference based novel and innovative approaches towards management of pests and diseases. She is heavily invested in research on nanotechnology for sustainable agriculture and is currently leading multidisciplinary consortia on global innovations for nanoparticle based delivery of actives/biomolecules/nucleic acids targeting plant and animal health.

Zhi Ping Xu

Zhi Ping Xu obtained his BSc degree from the University of Science and Technology of China (Hefei, China) in 1988, and received his PhD degree from National University of Singapore in 2001. After his postdoctoral fellowship at University of North Texas, he joined the Australian Institute for Bioengineering and Nanotechnology, the University of Queensland as a research fellow in 2004, and received promotions to senior research fellow and associate professor in 2008 and 2011, respectively. He has published over 190 journal papers, and his current research focuses on developing clay and clay-hybrid nanomaterials for health protection of humans, animals and plants through delivering drugs, genes, vaccines and/or nutrients, as well as for chemical catalysis.

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1. Introduction

Food is essential for the survival for human beings, and demands for food productivity and quality have continuously increased with the increase of the world population. Studies by plant physiologists have confirmed the occurrence of micronutrient deficiencies in food crops, which severely affects the food yield and quality.

To correct nutrient deficiencies, application of fertilizers has had a long history along with the development of human society. Besides the commonly applied macronutrient NPK fertilizers, micronutrient fertilizers have attracted more interest recently. Foliar fertilizers have been reported to have better uptake efficacy than the conventional soil ones,¹ though the mediating factors of leaf uptake are still unsolved.

With the rapid advancement of nanotechnology since the late stage of last century, controlled preparation of nanomaterials with desired morphology and size, and newly established concepts and methodology have underpinned the solid bases to solve the unsolved questions in foliar micronutrient uptake. From the view of surface chemistry and material science, the micronutrient ion uptake process is viewed as membrane transport – a complicated physicochemical process. The biodiversity of the plants is therefore neglected and the leaves are rather distinguished according to their surface morphology and properties, e.g. hydrophilicity/hydrophobicity, providing potential feasibility for efficient systematic statistics and modeling.

Interests on agricultural applications of nanotechnology have arisen for improved efficiency and productivity. Reviews are available for delivery systems and sensors,^2–4 while nanoscale agricultural chemicals, particularly foliar fertilizers, have not been covered yet. Thus, this review article summarises the latest development in foliar micronutrient fertilizers by employing materials nanotechnology, and then provides our perspectives in this prosperous area. Note that micronutrients and microelements are alternately used with the same meaning, mainly including Zn, Mn, Cu, Fe, Mo, B, and Cl in any forms and valence states in this review.

2. History of fertilizer application

2.1. History of fertilizers

Plants, at the bottom of the food chains, provide the essential nutrients to humans and animals. With the advancement of contemporary science and technology, increasing plant production per unit area is possible by screening better genotypes, planting with optimised density and timing, etc. Increasing application of the macronutrient fertilizers also promotes the productivity. However, the increase in crop productivity has come at a cost, including induced salinisation and desertification, which significantly aggravates the loss of available agricultural lands.

Fertilisation is the most commonly applied method to correct the nutrient deficiency. In the ancient document about agriculture written in 533–544 A.D. in China, fertilisation methodology had already been systematically introduced. Chemical fertilizers have been applied since early 19^th century when the first chemical fertilizer, superphosphate, was synthesised. Later on, Justus Freiherr von Liebig published “Organic Chemistry in its Application to Agriculture and Physiology” in 1840, which popularised the application of synthetic chemical fertilizers.⁵

2.2. Influence of micronutrient deficiency

Increasing number of reports have suggested that micronutrient deficiency around the world has become the major obstacle of agricultural crop productivity. This is because acute micronutrient deficiencies at a critical reproductive stage usually reduce the crop yield and quality, resulting in the short shelf life and the low market value.

Moreover, micronutrient deficiencies in crops may directly result in micronutrient deficiency in some populations, whose primary diet is cereal-based without adequate access to animal proteins, such as in southern Asia and some African countries. As an example, conservative estimates have suggested that 25% of the world's population is at risk of zinc deficiency.⁶ Incidence of prolonged labour, haemorrhage, uterine dystopia and placental abruption has been documented in zinc-deficient animals, while a review about pregnancy suggests that the human foetus is also susceptible to the teratogenic effects of severe zinc deficiency.⁷ Crop production is the primary industry in most developing countries with >60% of the world population.⁸ Thus, supply of sufficient micronutrients in food crops is critical and effective in preventing microelement malnutrition worldwide.

2.3. Advantages of foliar fertilizers to correct micronutrient deficiency

Foliar application has better efficiency to correct micronutrient deficiencies than macronutrient ones. The major advantages of foliar application is that the nutrient uptake directly occurs on the leaf, where all nutrients may be deployed, which helps avoid the disadvantages of soil fertilizers, such as phytotoxicity, loss in soil, slow response, and potential pollution. On the other hand, a much less demanded amount of micronutrients allows sufficient supply through leaves.

Field trials on commercial crops have suggested increases of yield,^9,10 nutrient concentrations^3,11 in plants, and reproductive efficiency¹² after foliar fertilizer application. Provided the drawbacks can be overcome with development of technology in engineering and materials science, the application of foliar fertilizers can provide a significant market prospect in the field of agrochemical engineering, as addressed shortly.

3. Micronutrients for plants

3.1. Physiological functions of micronutrients

There are seven micronutrient elements (Zn, Mn, Cu, Fe, Mo, B, and Cl) that are identified in the plant tissues. Despite their low concentration in plants, deficiency of these elements could cause failure of plant growth and reproduction. The correction of such deficiencies has attracted increasing attention from the researchers in agriculture and materials sciences. Deficiencies of zinc, manganese, copper and iron and the correction strategies are discussed in detail in this review paper.

Table 1 summarises the physiological functions, symptoms for deficiency and phytotoxicity of micronutrients, and present correction dosages in different methods. The blank block indicates that no corresponding report is found for the item. In addition, suggested human daily uptakes are also provided as the reference. It is noted that these four elements could be distinguished into two groups according to their chemical similarity: zinc/copper and manganese/iron.

Table 1 Functions, symptoms, and corrections of reviewed micronutrients

Items		Zn	Cu	Mn	Fe
a “D” = deficiency; “T” = phytotoxicity.b Dosages of elements.
Physiological functions	Carbohydrate metabolism	●^13	●^14	●^15	●^16
	Protein metabolism	●^13	●^17	●^18	●^19
	Structural integrity	●^20–22	●^23	●^24	●^25
	Auxin metabolism	●^26	●^27	●^28	●^29
	Defense	●^24	●^23	●^24	●^30
	Reproduction	●^31	●^32
	N metabolism	●^33	●^34	●^35	●^36
	Lipid metabolism			●^37	●^38
Symptoms^a	Chlorosis	D^39 T^40	D^41 T^42	D^43 T^44	D^36
	Growth inhibition	D^39 T^40	D^45 T^41	D^28 T^46	D^47
	Necrosis	D^39	D^41	D^48 T^49	D^50 T^51
	Discolouration	T^52		D^53
Correction^b ^54 (kg ha^−1)	Banding	2–22 ^55	1.1–6.6	5.6	30
	Broadcast	4.5–34	3.3–14.5	67.2	24
	Foliar	0.56–1.4	0.09–4.0	1–5	0.9–4.5
Human uptake^56 (mg day^−1)		5–20	0.4–3.0	0.3–5.0	7–27

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These microelements play important roles in structural integrity, defense, reproduction, and metabolism of nitrogen, lipid, carbohydrate, protein, and auxin of plants. Such items are pivotal throughout the plant growth, indicating the reviewed elements are essential though the demanded amounts are small. Interestingly, zinc and copper do not functionalise in lipid metabolism whereas manganese and iron are absent in reproduction, which coincide with their chemical similarity.

Chlorosis is the most common and easily identified symptom when plants are suffering deficiency of these elements. This is one of the reasons why these elements are categorised as essential elements because leaves are the sites of photosynthesis – the vital process for plant survival and growth. Growth inhibition and necrosis can also indicate deficiencies of all four elements. In addition, deficiency of manganese may induce discolouration.

By contrast, excessive uptake of these elements may incur similar symptoms as well. Chlorosis and growth inhibition could be observed as the consequence of phytotoxicity under excessive zinc, copper, and manganese. Necrosis could be induced by excessive manganese and iron. Purple stem and petioles of peanuts due to excessive zinc were reported as well.

Obviously, proper amounts of these microelements in plants ensure the normal growth and high production yield. In most cases, the micronutrient deficiency is more common than the phytotoxicity, so the deficiency correction is the major goal of new-generation foliar fertilizers.

3.2. Uptake pathways

Foliar absorption is a multi-step process. The leaf is covered by a non-cellular cuticular structure,⁵⁷ which acts as a barrier to external substances, as shown in Fig. 1A. The physical properties of the cuticle, e.g. thickness, weight, surface wax, and wettability, are essential to the penetration of the external substances.⁵⁸ Studies on the penetration of substances through the cuticle indicate that the process is passive and not energy-mediated.⁵⁹ The ions released from foliar fertilizers can only penetrate cuticle through the aqueous pores (Fig. 1B).⁶⁰

Fig. 1 (A) Apoplast pathway (red) and sympoplast pathway (black) of foliar uptake (this figure is modified from the work of http://www.MolecularExpressions.com at Florida State University with permission from Erik Clark), (B) ion pathway and lipid pathway through cuticle.⁶⁰

The substance moves along the apoplastic pathway of the cell walls of the epidermal and mesophyll cells, or is actively absorbed through the plasma membrane of the leaf cells and transported along the symplastic pathway within the cells, before reaching the phloem.⁶¹

Fertilizers landing on stems and flowers can also be utilised by plants. The mechanism is similar to that on leaves as the surface structures of stems and flowers are similar to that of leaves, which is commonly acknowledged in plant biology.

Several requisites are essential to the foliar uptake: (1) available form, i.e. ionic form for these microelements; (2) penetration through the cuticle; (3) reaching the target organ; (4) sufficient retention in the organ; and (5) nutrients transportable to the target tissue. The major penetration through the cuticle is a diffusive process and the main driving force for diffusion from outside into the leaf is the ionic concentration gradient between supplied water solution and the solution in apoplast space.⁶² Therefore this process is highly dependent on the physicochemical properties of the applied fertilizers.

3.3. Metabolic responses

Exploration of the metabolic responses to foliar fertilizers has been attracting research interests for better understanding of the uptake and translocation in plants. Papadakis et al. reported increased iron concentrations in basal leaves and stem and increased manganese concentrations in top and basal leaves and stem after foliar application of manganese sulphate and ferrous sulphate in two citrus genotypes.⁶³ Tian et al. focused on the zinc sequestration at the cellular level and suggested that the epidermal layers served as storage sites.⁶⁴ Fernández and Brown reviewed the major bottlenecks and expected better understanding of the governing factors.⁶⁵ Recently, Qiao et al. reported effect of zinc foliar spray on activity of enzyme, which could promote photosynthesis.⁶⁶

Studies of the effects of micronutrient foliar fertilizers on various plants have revealed positive outcomes.^10,67,68 Zinc deficiency is more popular worldwide and thus has attracted most attention. Keshavarz et al. assessed boron and zinc foliar applications and confirmed prompted vegetative and reproductive growth on walnut.⁶⁹ Johnson et al. compared the effectiveness of several soluble and less-soluble zinc formulations on peach seedlings and proposed that the higher the solubility and the smaller the accompanying anion, the better the effectiveness, but the more phytotoxic.⁷⁰ White et al. tested zinc foliar fertilizers on potatoes. They noted that 40-fold increase in shoot zinc concentration only afforded doubling in tuber zinc concentration, suggesting restricted zinc mobility in the phloem, which was supported by the comparative study involving nitrogen concentration in the tuber.⁷¹

Dordas reported improved cotton seed quality after foliar manganese application.⁷² Last and Bean also investigated controlling manganese deficiency with foliar sprays.⁷³ Different manganese fertilizers in soil and foliar applications had been compared.⁷⁴ The combined effect of foliar-applied manganese, zinc, and boron was found to be effective in reducing lesions by Simoglou and Dordas, though the mechanisms remain unknown.⁷⁵

Copper foliar fertilizer was relatively less studied due to its low demand and usually accompanying other nutrients.⁷⁶ Bernal et al. studied excessive copper supply and examined uptake and transport paths in the leaf, which is different from that in root.⁷⁷ Malhi et al. compared various sources, methods, times, and rates of copper fertilizers and suggested that foliar application may be the most practical and economical way.⁷⁸ Later Malhi and Karamanos reviewed utilisation of copper fertilizers in Prairie provinces of Canada.⁷⁹

Investigations on iron foliar fertilizers are of great interest due to the consequently high demand by animals and human.^4,80–83 Franzen et al. studied the interaction of foliar iron-EDTA and herbicides, but found that foliar iron-EDTA neither reduced chlorosis, herbicide injury nor increased the yield of soybeans.⁸⁴ Abadía et al. reviewed iron fertilizers for correcting chlorosis and plant response, and suggested further advancement in transport, xylem loading/unloading, immobilisation and acquisition of iron in various environments.⁸⁵ El-Jendoubi et al. assessed the effectiveness and efficiency of various iron fertilizers.⁸⁶ Recently, El-Jendoubi et al. observed relief of chlorosis only at the sprayed area after ferrous sulphate was applied, suggesting the in-leaf mobility of iron is a major constraint.⁸⁷ Comparison between different forms of foliar iron fertilizers suggested the chelates had better performance.^88,89 Combined effect with other nutrients has also been reported.^89–91 Zhang et al. investigated response of ginseng to foliar application of all four reviewed elements and found it was more sensitive to iron.⁹²

4. Current micronutrient foliar fertilizers

4.1. Current market

During the period of 1977–1985, the annual consumption of zinc fertilizer in Australia was 900–1700 tons, while consumption of manganese, copper, iron, boron, and molybdenum was 917–3080, 2620–3510, 267–1060, 41–182, and 78–223 tons, respectively.⁹³ Data after 1985 was unfortunately no longer recorded. However, with development in fertilizer production, increasing research interest and a better understanding of the necessity of micronutrients in plant growth by the fertilizer customers, it would be reasonable to predict that the demand for micronutrient fertilizers would significantly increase. Furthermore, with a better understanding of the advantages compared to the soil fertilizers, the market for foliar fertilizers will have become an important one in the fertilizer industry.

4.2. Chemical forms

The first-generation foliar fertilizers have applied the same chemicals that are widely used as soil fertilizers, e.g. in the case of zinc, zinc sulphate and zinc oxide.^9,71 Table 2 lists the foliar fertilizers that are available on the current market. The first ones in each box are most frequently applied. Soluble sulphates are the favourite ones due to the low cost and easy preparation. Zinc and copper chlorides are also used. Although the application is limited by the high cost, metal ions conjugated with organic chelates (such as EDTA, DTPA and EDDHA), are optional soluble fertilizers, and are effective as long as they could maintain the chelate form.⁵⁴

Table 2 Current micronutrient foliar fertilizers

		Zn	Cu	Mn	Fe
Inorganic	Soluble	Sulphate, chloride	Sulphate, chloride	Sulphate	Sulphate
	Less-soluble	Oxide, sulfide, basic sulphate, basic carbonate	Oxides, basic sulphate, basic carbonate	Carbonate, oxides	Oxide, hydroxide
Organic		Synthetic chelates, natural complexes	Chelates	Chelates	Chelates

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For less-soluble foliar fertilizers, oxides have high contents of desired elements and easy preparation, and are available for all four elements. Basic sulphates and carbonates of zinc and copper are also available and applied. Relatively, manganese carbonate is more common for element Mn. Private communication with fertilizer providers by the authors has revealed that fertilizers with the major component being iron oxide or iron oxide hydroxide have been produced, but the performance has not yet been tested.

The critical concentrations for deficiency and phytotoxicity of all four micronutrients have been summarised in Table 3. Note that CDC and CTC are dependent on the species and age of plants, so their values are in a range, not single values, as summarised from literature. Based on these data, we have proposed the desired concentration ranges in the 3^rd row. The current less-soluble fertilizers have been listed together with their solubility product (K_sp) constants. The experimental ion concentrations, measured by atom absorption spectroscopy (AAS), show that present less-soluble fertilizers cannot afford enough micronutrients to fulfil the demand of the plants under practical conditions, e.g. pH = 5–9, in foliar application.

Table 3 Critical concentrations of micronutrients and K_sp constants of current less-soluble fertilizers

Items	Zn	Cu	Mn	Fe
a CDC = critical deficiency concentration (mg kg^−1 dry weight in leaves).b CTC = critical toxic concentration (mg kg^−1 dry weight in leaves).c Ion concentration in suspensions estimated with the average water content in crop leaf = 70 wt%.d Provided by the industrial partner.e Solubility product (Ksp) constant data of Zn(OH)2, Cu(OH)2, and Fe(OH)2/Fe(OH)3.
CDC^a^94	15–30	1–3.5	10–15	30–50
CTC^b^94	200–500	15–30	100–5000	400–1000
Desired [M^2+]^c (mg L^−1)	10–100	1–5	5–100	20–100
Main components of common less-soluble fertilizers^d	ZnO	CuO	MnCO3	FeO/Fe2O3
Ion release from above fertilizers (mg L^−1)	2–4	<1	∼50	∼15
log Ksp^e^95	−16.1	−19.5	−10.65	−14/−42.7

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4.3. Challenges for new-generation foliar fertilizers

The new-generation foliar fertilizers are expected to be of suspension form, containing nanoparticles with balanced soluble microelement ions, which is sufficient to instantly correct deficiency but does not reach the phytotoxic level. Once sprayed on the leaf, the existing ions are effective instantly until the droplets are dried out by evaporation, with the nanoparticles steadily residing on the leaf surface. When dew water condenses on the leaf surface every dawn, the nanoparticles dissolve and release microelement ions through the dissolution/precipitation equilibrium, achieving the concentration gradient needed to trigger foliar uptake of microelement ions, until the dew droplets are dried out again. This cycle should keep acting spontaneously until the nanoparticles on the leaf surface are completely consumed after 4–6 weeks.

In our opinion, there are several challenges in development of new-generation foliar fertilizers:

(1) Solubility of nanocrystals.

(2) Residence fastness on the leaf surface.

(3) Distribution of fertilizer particles on the leaf surface after drying.

(4) Methodology for assessing the effectiveness.

As schematically illustrated in Fig. 2, the soluble fertilizers can rapidly correct the deficiencies after spraying. However the plants will again struggle due to the lack of continuous supply and soon return to a deficient state if repeating spraying is not afforded. In the field trials on commercial crops utilising soluble fertilizers and biostimulant, the micronutrient concentration had a little but no significant increase, while the yield was lower than those treated by biostimulant only.²

Fig. 2 Schematic performance of current and future foliar fertilizers.

Multiple supplies of soluble fertilizers were reported to effectively increase the micronutrient concentration in plants.^3,9 However, the application of a soluble fertilizer at a high concentration usually leads to phytotoxicity and therefore can only be conducted at a low concentration through multiple sprays to supply adequate nutrients for crop growth, which inevitably induces a high labour cost.

Current less-soluble foliar fertilizers, on the other hand, are inorganic mineral compounds (e.g. oxides, hydroxides and carbonates), which are finely ground and have very low aqueous solubilities (Table 3), thus allowing growers to spray at much higher loadings on plant leaves than the soluble fertilizers. However, such less-soluble fertilizers cannot afford the timely supply of enough microelement ions to correct the deficiency (Fig. 2). Hence, the physiological activities of plants are always kept in a weakly activated state.

As the residence time on leaves extends, climate influences become increasingly greater. Less-soluble fertilizers, especially those designed and prepared without consideration of adhesion, will be readily blown away by wind or flushed off from the leaves to soils by rain.

Despite development of suspension technology, the effectiveness of less-soluble foliar fertilizers is somewhat limited further due to other characteristics, such as poor distribution of fertilizer droplets and low dissolution of fertilizer minerals on leaf surfaces. Such disadvantages have become major obstacles in the development of new-generation foliar fertilizers. To overcome these obstacles, factors mediating the uptake process need to be understood, which unfortunately remain unresolved.

Another challenge is the method for comparing the efficacy between the soluble fertilizers and less-soluble ones. The low solubility of the less-soluble one could allow a high foliar dosage, while the soluble one at that dosage would burn the leaves. From the opposed point of view, suitable dosage for soluble one would not allow less-soluble fertilizer to provide a long term supply of enough microelement ions on the leaves. Therefore a better method to quantitatively analyse the foliar uptake of micronutrient from suspensions is essential to identifying the efficacy of long-term foliar fertilizers.

5. Nanotechnology in R&D of micronutrient foliar fertilizers

5.1. Nanotechnology and agriculture

Since its emergence in the 1980s, nanotechnology has been applied mainly in the fields of electronics, energy, medicine and life science, and catalysis. The experiences can be borrowed to broaden novel applications in agriculture, particularly, for the new-generation foliar fertilizers.

Direct applications of nanotechnology in plant-based agricultural production and products mainly include delivery of agrochemicals and pesticides, study of plant disease mechanisms, genomes improvement, and lignocellulosic nanomaterials.⁹⁶ Among these applications, efforts on nanomaterials have been mainly focused on smart delivery.^97,98

The ideal nanomaterials for agricultural applications are supposed to have the following properties: providing effective concentration and controlled release of nutrient elements or pesticides in response to certain stimuli, enhanced targeted activity, and less ecotoxicity with safe and easy delivery.⁹⁹

Foliar fertilizers are one of such applications that are tightly related to the advancement of nanotechnology. A persistent issue limiting the foliar effectiveness is the adhesion of fertilizer particles on the limited area of the leaf surface, which is relevant to the particle morphology and size. Nanotechnological concepts and methodology can be used to prepare fertilizer crystal products with controllable morphology and particle size, therefore improving the adhesion fastness. Moreover, crystal fertilizers can be made in the nanometre scale so as to slowly release metal ion in a lower equilibrated concentration for a longer term, which would be ideally suitable for ion penetration into the leaf but not cause any considerable phytotoxicity.

Reports concerning nanomaterial impacts on the plant metabolism have been increasing in recent years, among which concerning foliar uptake of nanoparticles is still limited, and has dispute. Birbaum et al. claimed no evidence of nanoparticle translocation in maize plants in 2010.¹⁰⁰ In contrast, more and more studies have reported foliar uptake of nanoparticle through stomatal pathway.^101–103 Zhu et al.¹⁰⁴ and Corredor et al.¹⁰⁵ reported evidence of penetration and transport of coated magnetic nanoparticles in living pumpkin. Fernández and Eichert proposed that recent advances in materials, aerosol, and nanotechnology could enhance the research progress of foliar fertilisation.¹⁰⁶ For example, Wang et al. reported that aerosolised nanoparticles more easily entered stomata than those in liquid phase.¹⁰⁷ No matter whether the nanoparticles enter the leaf, we believe that ion penetration (Fig. 1B) should be the major way for the leaf to take up the microelements.

5.2. Desirable foliar fertilizers

In Shoji and Gandeza's opinion,¹⁰⁸ an ideal fertilizer should have at least the following three characteristics:

· Only one single application throughout the entire growing season,

· High maximum percentage recovery, and

· Minimum detrimental effects on soil, water and atmospheric environments.

Regarding new-generation foliar fertilizers, we have thus proposed the particular desired properties as follows:

(1) Suitable aqueous solubility to provide sufficient microelement ions to correct both instant and long-term deficiencies.

(2) Sheet-like or platelet-like morphology to provide more specific contact area and, consequently, strong adhesion.

(3) Compatible surface properties to provide enhanced interactions between the leaf surface and fertilizer particles via electrostatic, hydrophobic and van der Waals forces.

(4) Suitable additives to aid ready condensation of dew water.

(5) Easy preparation at a reasonably low cost in the industrial scale.

As proposed in Table 3, the ion concentrations in the fertilizer suspensions should be higher than the critical deficiency concentrations to acquire the concentration gradients and drive the instant occurrence of foliar uptake. Also, the ion concentration should be lower than the critical toxic concentrations simply to avoid phytotoxicity. Table 3 lists the desired ion concentration range for each element, while the exact value for each element may vary depending on the target crops.

The morphological and size effects on the adhesion of fertilizer particles on the leaf surface have rarely been considered in the design and manufacture of fertilizers in the past, but they are essential to the total effectiveness and efficiency.

As illustrated in Fig. 3, sheet-like or plate-like particles have the highest specific contact area and the least mobility on the leaf surface assuming that the leaf surface is flat. In comparison, the other two typical morphologies seem to have much less contact area, and thus the particles would have weaker adhesion onto the leaf and much more easily fall off due to wind and/or rain.

Fig. 3 Schematic hypothesis of morphological effect on foliar residue of fertilizers.

Moreover, the concepts and theories from surface science and materials science can be used to modify the surface properties of fertilizer particles to suit the leaf surface characteristics and reinforce the adhesion and extend the residence time on the leaf surface. For instance, leaf cuticles are composed of biomolecules with the carboxylic groups, so the leaf surface carries negative charge at neutral pH.¹⁰⁶ Therefore, fertilizer particles with positive surface charges would adhere to the leaf surface more strongly than those with negative charges.

The wettability is critical to the daily dissolution of fertilizer particles by dew water, demanding suitable point of deliquescence (POD). If POD is too high, surface modification would be necessary to decrease the POD and readily condense more dew water, which would help dissolve foliar fertilizer particles to provide more ions for the leaf to take up.

5.3. Recent development of new-generation foliar fertilizers

Based on the proposed desirable properties for next-generation foliar fertilizers, we have conducted the research on developing some novel fertilizers in the last several years, including those containing Zn, Cu, Fe and Mn elements, as briefly reviewed below, taking Zn as an example.

Zinc hydroxide nitrate, with brucite-like crystal structure, sheet-like morphology, and characteristic coordination of nitrate groups,¹⁰⁹ was first proposed for Zn foliar fertilizer candidate. Its peculiar property other than Zn(OH)₂ is its suitable solubility estimated and measured (∼40 mg L⁻¹ in Table 4 vs. 2–4 mg L⁻¹ in Table 3), which would meet the demand for zinc deficiency correction (Table 3).

Table 4 Summary of synthesised long-term micronutrient foliar fertilizers

	Synthesised compounds	log Ksp	[M^2+]^a (mg L^−1)	Morphology	Size (nm)	Thickness (nm)
a Tested by atomic absorption spectroscopy.
Zn^110	Hydroxide nitrate	−13.6	∼37	Sheet-like	∼500	∼20
Cu + Zn^120	Hydroxide nitrate	—	Zn: ∼40, Cu: ∼4	Sheet-like	∼300	∼20
	Hydroxide sulphate	—	Zn: ∼40, Cu: ∼1	Sheet-like	∼300	∼30
Mn(II)^121	Ammonium phosphate	−12.0	∼10	Sheet-like	∼3000	∼200
	Oxalate	−5.3	∼110	Sheet-like	∼500	<20
Fe(II)^121	Ammonium phosphate	−10.8	∼10	Sheet-like	∼4000	∼200
	Oxalate	−6.5	∼30	Irregular	—	—

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Zinc hydroxide nitrate was prepared from zinc nitrate and sodium hydroxide.¹¹⁰ Fig. 4 demonstrates the XRD patterns, FTIR spectra, and SEM images of zinc hydroxide nitrate, zinc hydroxide and zinc oxide. The crystal phases were confirmed by the XRD patterns and the FTIR spectra, and the SEM images showed the typical sheet-like morphology of zinc hydroxide nitrate. These characteristics demonstrate that zinc hydroxide nitrate appears to be the target Zn fertilizer, and can be readily obtained after 1 h ageing after mixing zinc nitrate and sodium hydroxide.

Fig. 4 XRD patterns, FTIR spectra, and SEM images of zinc hydroxide nitrate, zinc hydroxide, and zinc oxide, prepared from zinc nitrate and sodium hydroxide at OH/Zn molar ratio = 1.6 for different ageing time.¹¹⁰ (This figure is reproduced from ref. 110 with permission from Li et al.)

We then investigated the deposition patterns of one commercial zinc foliar fertilizer (Activist Zn, main component is ZnO, with some surfactants) and zinc hydroxide nitrate (Fig. 5). The image of the commercial product shows a clear “coffee ring” pattern where the particles accumulated in a limited area and had poor contact with the leaf surface (Fig. 5a). Such a deposition pattern is not favourable for efficient particle dissolution and resistance against the wind blowing and raining washing. By contrast, zinc hydroxide nitrate particles formed a well-spread pattern with much larger contact surface area (Fig. 5b). Better adhesion and higher efficiency of dissolution could therefore be expected.

Fig. 5 On-leaf deposition pattern of (a) commercial zinc foliar fertilizer (ZnO-based Activist Zn) and (b) zinc hydroxide nitrate.

The performance of zinc hydroxide nitrate was further compared with Activist Zn on cultivated detached leaves of citrus, capsicum, and tomato, respectively, as shown in Fig. 6. On all three kinds of plant leaves, the foliar uptake of zinc ions from zinc hydroxide nitrate was 30–40% higher than that from the commercial product (Fig. 6).

Fig. 6 Foliar uptake of zinc from zinc hydroxide nitrate and Activist Zn (ZnO-based) on the leaves of citrus, capsicum, and tomato.

We have also used a cation exchange membrane to simulate the leaf surface and evaluated the sustainable ion release from our target fertilizer. The humidity was set on the saturated level in the laboratory setup to assure the water condensation and fertilizer particle dissolution. Fig. 7 shows that the zinc release from zinc hydroxide nitrate continued for 6–8 days. Considering that dew water could last 4–6 h per day on the leaf surface and dissolve zinc hydroxide nitrate particles to release zinc ions, it is reasonable to estimate that zinc hydroxide nitrate particles could remain effective for 4–6 weeks on the leaf surface if the dosage is similar to this simulation.

Fig. 7 Simulated Zn²⁺ release from zinc hydroxide nitrate on cation exchange membrane under saturated humidity.

Comparison between zinc hydroxide nitrate and zinc nitrate was also conducted on tomato leaves to verify the different plant responses to less-soluble and soluble foliar fertilizers.¹¹¹ Within the 3 weeks, total Zn recovery was ∼16% and ∼90% from plants treated with zinc hydroxide nitrate and zinc nitrate applied, respectively. Distribution of foliar-absorbed zinc to other plant parts in zinc-deficient plants, preferentially to the roots (to generate a larger root system for a higher chance of Zn absorption from soils), was observed. The data (Fig. 8) demonstrate that zinc ions were gradually released from less-soluble foliar fertilizer over a certain growth period at a rate slower (but quantitatively effective) than zinc nitrate. Spraying of zinc hydroxide nitrate suspension on a larger leaf surface area could enhance the efficacy of the prolonged foliar Zn supply at the peak vegetative or early flowering stage. Note that the Zn concentration in zinc nitrate solution was 400 mg L⁻¹, which may cause some phytotoxicity (Table 3), while that in zinc hydroxide nitrate suspension was kept at 40 mg L⁻¹ (Table 4 although the applied suspension contained 400 mg L⁻¹ Zn), suitable for continuous uptake by the leaves for a longer term.

Fig. 8 Zinc contents (μg) in (a) shoot tip, (b) leaves between shoot tip and treated leaf, (c) stem segment 1, (d) treated leaf, (e) stem segment 2, (f) stem segment 3, (g) root, and (h) flower in response to foliar treatments of 400 mg Zn per L zinc hydroxide nitrate suspension or zinc nitrate for three weeks. Data present means ± SE of four replicates. The values labelled with same letter were not significantly different at Fisher's LSD 95%. (This figure is reproduced from ref. 111 with permission from Du et al.)

Characterisation methods via spectroscopic study such as XRF are able to afford understanding of the in-plant transport of the micronutrients.^64,112–114 Australian Synchrotron beamline was adopted to verify the uptake of zinc from zinc hydroxide nitrate suspension (Fig. 9).¹¹⁵ The results showed 2- to 10-fold higher “local” concentration than in the adjacent tissues, indicating strong in-leaf binding of zinc with limited redistribution in low-order veins. While in high-order veins, zinc movement was comparatively limited as well, with concentrations decreasing to background levels, which is in contrast to root-applied zinc that forms complexes with ligands.¹¹⁶ Such limited movement of foliar-applied zinc is attributed to high binding capacity of leaf cells,¹¹⁷ and/or limited/conditional mobility in the phloem.¹¹⁸ However, a peer report¹¹⁹ and our glasshouse experiments suggested that it is still sufficient to increase both shoot and root mass substantially in Zn-deficient plants.

Fig. 9 Youngest full expanded leaf (normal Zn status) of tomato sprayed with zinc hydroxide nitrate (ZHN) on both sides of the surfaces and determined by μ-XRF.¹¹⁵ (This figure is reproduced from ref. 115 with permission from Du et al.)

Therefore, our research has altogether demonstrated that zinc hydroxide nitrate crystal is a very potential effective foliar fertilizer as it has a suitable solubility (∼40 mg L⁻¹ Zn²⁺), a sheet-like morphology and a surface suitable for even deposition on the leaf surface. Moreover, the uptake of Zn ions from this crystal by three kinds of leaves is 30–40% enhanced compared with the commercial zinc foliar fertilizer.

Apart from zinc hydroxide nitrate, zinc hydroxide sulphate has been also demonstrated to be another potential zinc foliar fertilizer. In particular, we prepared Cu–Zn mixed hydroxide nitrate/sulphate for a dual microelement foliar fertilizer (Table 4). Considering the low demanding amount of copper by plants, Cu–Zn mixed hydroxide nitrate/sulphate crystals contained much less Cu (15–20% Cu and 85–80% Zn), with the sheet-like morphology (Fig. 10).¹²⁰ More interestingly, the Zn²⁺ and Cu²⁺ concentration in the suspension was ∼40 and 1–4 mg L⁻¹ (Table 4), respectively, meeting the proposed demand for correcting deficiency of both microelements.

Fig. 10 TEM/SEM images of: (a) (Cu–Zn) hydroxide nitrate, (b) (Cu–Zn) hydroxide sulfate, (c) Mn(II) ammonium phosphate, (d) Mn(II) oxalate, (e) Fe(II) ammonium phosphate, and (f) Fe(II) oxalate.^120,121 (This figure is reproduced from ref. 120 and 121 with permission from Li et al. and Li et al.)

We have also prepared the basic salts of manganese(II) and iron(II). However, Mn(II) and Fe(II) are easily oxidised in the ambient environment, and are not ideal as foliar fertilizers. Thus, we attempted to maintain the valence stability by preparing ammonium phosphates and oxalates of Mn(II) and Fe(II).¹²¹ The crystals phases were confirmed by XRD and FTIR. Clearly, their solubility was all suitable, as summarised in Table 4.

As shown in Fig. 10, the morphology of these synthesised crystals was mostly sheet-like, except Fe(II) oxalate, which needs further processing. The nanoscale thickness can provide large specific contact area with the leaf surface, and consequently prompt the attachment.

To summarise, we have designed and developed several crystals as potential foliar fertilizers, whose ion release levels are falling in the proposed ranges (Table 3). Their morphologies are mostly sheet-like or platelet-like. New methods have been developed to provide comparison between compounds with different levels of solubility to demonstrate the efficacy and efficiency of these potential long-term micronutrient foliar fertilizers.

6. Future perspectives

With the efforts contributed to developing long-term foliar fertilizers for zinc, manganese, copper, and iron, the authors are establishing a practical and economical operation procedure, from compound selection to performance evaluation, which could be applied in development of long-term foliar fertilizers for other micronutrients when necessary.

There still remains a lot of further research using nanotechnology to develop more effective foliar micronutrient fertilizers. As presented previously, we have been pioneering the research in this field, and many efforts will be made to develop new-generation micronutrient foliar fertilizers. In our opinion, there would be more nanocrystals to be designed and developed with suitable solubility and morphology. Moreover, more attention should be paid to the surface modification using various biopolymers in order to enhance the stickiness of the crystals onto the leaf surface. The crystal-leaf surface interactions could be strengthened by match-making their physicochemical properties. More glasshouse experiments that simulate raining or winding are needed to clearly correlate the sticky fastness of the fertilizer crystals on the leaf surface with their size, morphology, and surface properties.

Another practical challenge is mainly attributed to environmental factors induced by the longer residence time of the fertilizers on leaves. Whether the fertilizer particles can steadily stay on leaf surfaces is vital for evaluating the effectiveness and performance. Therefore, evaluation methods for the fastness against rain and wind are demanded. The results could clearly instruct the practical application, e.g. what levels of rain or wind require re-application of suspension foliar fertilizers afterwards. Theories and functions of computational fluid dynamics and aerodynamics could be applied to establish this evaluation system by involving the statistical data of the regional climate. With such a system accomplished, researchers could investigate more extensively on the effectiveness of long-term foliar fertilizers. In-depth and long-term field trials are required globally to observe the practical environmental behaviour and ecotoxicity of nanoparticles.¹²²

Functions, risks, and compatibilities of potential additives as well as their combinations need extensive investigation. Various formulations of additives are necessary to affiliate the different kinds of local climate parameters, in order to maximise the dew water condensation on the leaf surface and subsequent micronutrient foliar uptake. Collaboration with meteorologists could be established. By adding feathers of additive properties into the present meteorological data and model, formulations for defined area could be proposed by computer software.

Acknowledgements

This material is based on work supported under Australian Research Council's Linkage Project (LP0989217) and covered by the Australian Patent 2011900756. We would like to thank Tuan A. H. Nguyen, Anh Nguyen, Mark Hampton, and Victor Rudolph for their contribution in the manuscript. Xu thanks the fund from the Australian Research Council (ARC) through Future Fellowship (FT120100813). The authors also appreciate the kind permission from Erik Clark, “http://www.MolecularExpression.com” at Florida State University for adopting their work in this manuscript.

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