Toward the Recent Advances in Nutrient Use Efficiency (NUE): Strategies to Improve Phosphorus Availability to Plants

Abstract

Achieving high nutrient use efficiency (NUE) and high crop productivity has become a challenge with increased global demand for food, depletion of natural resources, and deterioration of environmental conditions. Higher NUE by plants could reduce fertilizer input costs, decrease the rate of nutrient losses, and enhance crop yields. Nitrogen and Phosphorus are the most limiting nutrients for crop production in many of the world’s agricultural areas, and their efficient use is important for the economic sustainability of cropping systems. Furthermore, the dynamic nature of N and P in soil-plant systems creates a unique and challenging environment for its efficient management. Although numerous fertilizer recommendation methods have been proposed to improve NUE, technologies and innovative management practices are still lacking. Therefore, maximizing crop phosphorus (P) use efficiency (PUE) would be helpful in reducing the use of inorganic phosphorus fertilizers and their escape in the environment for sustainable agriculture. Improvement of PUE in cropping systems can be achieved through two main strategies: optimizing agronomic practice and breeding nutrient efficient crop cultivars that improves P-acquisition and -utilization efficiency. These strategies are needed for future food security and sustainable agriculture. The major revised points are the following: concept of NUE, application of nutrient stewardship, cereal-legume intercropping, regulating soil pH, etc., for enhancing phyto-availability of P and breeding P-efficient crop cultivars that can produce more biomass with lesser P costs and that acquire more P in P-stress condition. These approaches consider economic, social, and environmental dimensions essential to sustainable agricultural systems and afford a suitable context for specific NUE indicators.

1. Introduction

For sustainable food production, it is an absolute requirement that nutrients removed with the harvest of crops are replaced to prevent nutrient depletion and soil degradation. Achievement and maintenance of high nutrient use efficiency (NUE) together with high crop productivity have become a major challenge in both developed and developing countries with an increasing growing population, depletion of natural resources, and deteriorating environmental conditions. This is occurring at the same time as society becomes ever more concerned about resource management practices and the environment, especially when it comes to nutrient management [1]. Fertilizer nutrients applied that are not taken up by the crop are also vulnerable to losses from leaching, erosion, and denitrification or volatilization in the case of N, or they could be temporarily immobilized in soil organic matter to be released at a later time, all of which impact apparent use efficiency [2].

Improving nutrient use efficiency (NUE) in plants is vital to enhance the yield and quality of crops, reduce nutrient input cost and improve soil, water, and air quality [3]. Higher NUE by plants could reduce fertilizer input costs, decrease the rate of nutrient losses, and enhance crop yields. Improving crop nutrient use efficiency ideally requires an understanding of the whole system, from the macro (agro-ecosystem) to the molecular level [4]. Nutrient uptake and their internal utilization efficiencies are the two central cores for improving crop NUE [5]. This can be achieved through optimizing agronomic strategies (soil-rhizosphere management) and breeding nutrient-efficient cultivars. Plant genetics and physiological mechanisms and their interaction with best agronomic practice are also a tool that can be used to increase efficiency of cropping systems [3]. Thus, it needs involvement of integrated nutrient management strategies that take into consideration improved fertilizer along with soil and crop management practices are necessary [6]. Sustainable nutrient management must be both efficient and effective to deliver anticipated economic, social, and environmental benefits.

Plants experience nutrient deficiency when soil nutrient availability is either an inherently low amount or low mobility of nutrients in the soil, or poor solubility of certain chemical forms of soil nutrients [7]. Of the various nutrients essential for plants, nitrogen (N), phosphorus (P), and potassium (K) are required in the largest quantities, and their deficiency severely limits crop yield [8]. The dynamic nature of N and P in soil-plant systems creates a unique and challenging environment with nitrate and phosphate contamination of surface and/or groundwater, which can be attributed in large part to low efficiency in plant nutrient uptake. The main challenge for improving P and K use efficiency at the farm level is to apply the existing knowledge in a practical manner [9]. Hence, the best management practice for N, P, and K must consider the specific characteristics of crops, cropping systems, environments, and soils is application of 4R nutrient stewardship. Therefore, this chapter tries to summarize the concept of NUE and recent strategies for enhancing use efficiency of N, P, and K. These approaches consider economic, social, and environmental dimensions essential to sustainable agricultural systems and afford a suitable context for specific NUE indicators.

2. Concept of phosphorus use efficiency (PUE)

The variations in defining nutrient efficient plants and methods used in calculating nutrient use efficiency make it difficult to compare results of different studies [10, 11, 12, 13]. Understanding the terminology and the context in which it is used is critical to prevent misinterpretation and misunderstanding and determination of NUE in crop plants is an important approach to evaluate the fate of applied chemical fertilizers and their role in improving crop yields. In order to develop a common framework for NUE, scientists started to formulate concepts and definitions that should serve as a basis for comparison and discussion of research. Nutrient use efficiency in its broadest sense indicates how effectively a plant is able to capture and utilize nutrients to produce biomass. It is simply a measure of how well plants use the available mineral nutrients [10]. The earlier definition of NUE by [14] is simply increment of yield per applied nutrient (Eq. (1)).

$$\mathit{NUE}=\frac{\text{Total productivity}\left(\mathrm{g}{\mathrm{cm}}^{-2}{\text{year}}^{-1}\right)}{\text{Rate of resource uptake or acquisition}\mathrm{by}\text{plant}\left(\mathrm{g}\mathrm{N}{\mathrm{m}}^{-2}{\text{year}}^{-1}\right)}$$E1

While the most recent and complicated one used in crop modeling formula is (Eq. (2)) [12].

$$\mathit{NUE}=\frac{\left(R_{\mathit{ac}}-R_{\min }\right)\ast {\mathit{NPP}}_{\max }}{\left(R_{\mathit{ac}}-R_{\min }+\alpha \right)\ast N_{\mathit{ac}}}$$E2

where R_min is the estimated minimum resource requirement for positive growth, N_ac is the amount of nutrient uptake by plant, NPP_max is the production asymptote, and ∝ is the half-saturation constant with respect to resource.

Generally, nutrient use efficiency comprises both yield as a function of inputs and percentage of nutrient recovered respectively, contributing to yield and quality [15]. The NUE is based on (a) uptake efficiency (acquire from soil, influx rate into roots, influx kinetics, radial transport in roots are based on root parameters per weight or length, and uptake is also related to the amounts of the particular nutrient applied or present in soil), (b) incorporation efficiency (transports to shoot and leaves are based on shoot parameters), and (c) utilization efficiency (based on remobilization, whole plant, i.e., root and shoot parameters) [4].

Phosphorus use efficiency can be divided into (i) P acquisition efficiency [the capacity of a cultivar to extract P from soil] and (ii) P internal utilization efficiency [the capacity of a cultivar to transform the acquired P into biomass/grain yield] [16, 17, 18].

1. Phosphorus uptake or acquisition efficiency (PACE)

   Uptake efficiency or the ability of the plant to extract the nutrient from the soil is calculated as [19] (Eq. (3)).

   $$\mathrm{P}‐\text{uptake efficiency(PACE)}=\frac{\text{Total above}-\text{ground nutrient}\left(\mathrm{P}\right)\text{in the plant}\mathrm{at}\text{maturity}\left(\mathrm{Nt}\right)}{\text{Nutrient}\left(\mathrm{P}\right)\text{supplied}\left(\mathrm{Ns}\right)}$$E3

2. Phosphorus utilization efficiency (PUTE)

   Phosphorus utilization efficiency is defined as a crop’s ability to convert the absorbed P into grain yield [19] (Eq. (4)) can be calculated as:

   $$\mathrm{P}‐\text{utilization efficiency(PUTE)}=\frac{\text{Total above}-\text{ground plant}\mathrm{dry}\text{weight}\mathrm{at}\text{maturity}\left(\mathrm{Tw}\right)}{\text{Total aboveground plant nutrient}\mathrm{at}\text{maturity}\left(\mathrm{Nt}\right)}$$E4

Utilization efficiency can also be calculates as suggested by [20], (Eqs. (5) and (6)) and expressed as follows:

$$\text{Utilization efficiency}=\text{Harvest index}\times \text{Nutrient biomass production efficiency}$$E5

$$\text{Utilization efficiency}=\text{Harvest index}\times \text{Inverse of total nutrient concentration in the plant.}$$E6

Generally, if P supply is limited or in more acidic and calcareous soil, P acquisition could be more important than P utilization and high fertilizer application necessary in order to provide sufficient plant-available P. On the other hand, with adequate P supply, PUTE could be considered more important than PACE for crop P efficiency [17]. Therefore, the improvement of both PACE and PUTE in the given species under different P supply conditions in the different soil types seems to be the perfect breeding approach (Figure 1) [17].

Figure 1.

Schematic representation of the possible mechanisms of P acquisition and utilization for better growth of modern crops grown in intensive cropping systems (adopted from [17]).

Hence, Nutrient use efficiency = Uptake efficiency × Utilization efficiency. All unit dry weights are in g m⁻² [19].

For nitrogen use efficiency in their various definitions and components (Figure 2) [21].

Figure 2.

Illustration of nutrient use efficiency parameters exemplified by NUE in wheat. Key process contributing to the NUE trait: nitrogen uptake efficiency, NUpE; nitrogen utilization efficiency, NUtE; nitrogen harvest index, NHI (adopted form [15]).

Apparent recovery efficiency is one of the more complex forms of nutrient use efficiency (NUE) expressions and is most commonly defined as the difference in nutrient uptake in above-ground parts of the plant between the fertilized and unfertilized crop relative to the quantity of nutrient applied. It is often the preferred NUE expression by scientists studying the nutrient response of the crop [22]. Reference [23] proposed that the balance method be used to assess fertilizer P efficiency (Eq. (7)). The balance method is described mathematically as:

$$\mathrm{P}‐\mathrm{use}\text{efficincy}\left(\%\right)=\frac{\mathrm{P}\text{taken}\mathrm{up}\mathrm{by}\text{crop}\left(\text{fertilized soil}\right)}{\text{Amount of}\mathrm{P}\text{applied}}\times 100$$E7

3. Why we worry of phosphorus use efficiency

Phosphorus use efficiency has become burning issues in recent times due to several reasons [24]. Unlike N, the amount of P is less-abundant, finite resource, less-available, and poor mobility in the soil, being one of the most inaccessible elements for plants. Its deficiency is a major constraint to agricultural production, and it affects an area of over 2 billion hectares worldwide that is on about 70% of the world’s arable land [25]. Remarkably, usually only about 10–30% of the P fertilizer applied in the first year is taken up by the roots, with a substantial part accumulated in the soil as residual P not readily available for plants [26]. This may be due to nature of P that can bound to calcium in alkaline soils and readily complexed to charged Al and Fe oxides and groups hydroxyls on clay surfaces in acidic soils [23]. In addition, agricultural phosphorus (P) run-off is a primary factor in the eutrophication of aquatic and marine ecosystems and has also led to blooms of toxic cyanobacteria [27] and can contain heavy metals such as cadmium that may accumulate in arable soils. Moreover, organic material present in the soil (e.g., from manure or crop residues) can also bind phosphate ions as well as phytate (inositol compounds). In order to avoid a future food-related crisis, phosphorus scarcity needs to be recognized and addressed in contemporary discussions on global environmental change and food security, alongside water, energy, and nitrogen [28].

4. Breeding or crop modification strategies

4.1 Selection of improved genotypes

Selection and breeding nutrient-efficient species or genotypes within a species are justified in terms of reduction in fertilizer input cost of crop production and also reduced risk of contamination of soil and water. Many plants have evolved morphological, physiological, biochemical, and molecular adaptive systems to cope with P-deficiency stress, such as altered root architecture to explore more soil volume and increased carboxylate exudation containing phosphatases, nucleases, and various organic acids [29]. These mechanisms and strategies are necessary to liberate or solubilize Pi from organic and other insoluble pools [30], enhance Pi uptake capacity [31], recycle internal Pi remobilize/retranslocate P from mature to young developing organs [32, 33], and reprioritize metabolic P utilization [34]. Under the current situation, farmers need P-efficient genotypes that perform better than other genotypes with equivalent P inputs. Therefore, selection/identification of cultivars that can absorb and use P efficiently is a promising strategy to cope with environments deficient in bio-available P. Due to the diverse functional and structural roles of P in plants, P-use efficiency (PUE) is a complex trait to dissect [24].

4.2 Modification of root morphology and physiology

The root morphological factors such as length, thickness, surface area, and volume have profound effects on the plant’s ability to acquire and absorb nutrients in soil [35]. These parameters are influencing the ability of the roots to penetrate high density soil layers, to extremes tolerate temperature, moisture, toxicities, and deficiencies of elements. Additionally, they have the ability to modify the rhizosphere pH and the nutrient uptake kinetics. Efficient acquisition will depend first on root architecture in terms of transporters and exudates and often the presence of symbiotic associations such as mycorrhiza. Hence, improving early root establishment, high-affinity transporter systems, association of microorganisms (mycorrizha), proliferation of roots, and enhanced mechanisms for increasing bio-availability of nutrients and then enhancing NUE [5]. Improvement of transporters plays essential roles particularly in conjunction with effective root proliferation in contributing to nutrient use efficiency. The other important attribute for uptake efficiency is having adequate sinks to store acquired nutrients, which will prevent negative feedback regulation on the initial acquisition/assimilatory processes and should provide important remobilizable storage [5]. The second component of uptake efficiency is root physiological activity such as differing uptake kinetics, i.e., maximum net influx (I_max), affinity of the transporter (K_m) and the roots depletion ability (C_min), which result in different nutrient uptake rates per unit root and time due to their effect on P diffusion [36]. Lower Km values (higher affinity) and higher I_max values indicate a higher uptake rate of plants for a determined nutrient at low concentration [11].

A recent study further showed that root tips also play an important role and, despite their small size, accounted for approximately 20% of the total seedling Pi uptake [37], mainly increasing organic acid exudation strategies [38]. Plants increase total soil exploration by increasing root length, increasing root branching, increasing specific root length (i.e., roots with smaller diameter), and modifying branching angle [39, 40, 41]. The findings of Bates and Lynch [39] suggested that increased root growth is associated with improved plant performance under low P by exploring a larger volume of soil. Consequently, root: shoot ratio increases significantly in low-P environments and is an excellent index for partitioning photosynthesized carbon between above- and below-ground plant parts. Root density and root: shoot ratio generally increased under P deficiency, thus favoring P acquisition by plants [29].

Genetic variation for root hair traits, particularly root hair length, can be exploited in breeding for improved P uptake efficiency and P fertilizer use efficiency in crops. Moreover, a deeper root with more aerenchyma tissues in the cortex of the roots can also be an important trait that contributes to efficient N uptake with lower carbon input in root growth [42]. This root architecture may also be efficient in the uptake of deep water and therefore help to increase drought resistance [43]. However, Miguel et al. [44] showed in field trials that shallow and hairy root traits are synergistic in their effects on Pi uptake by bean. However, modifying root growth in response to nutrient deficiency, it is a challenge and complex to identify key regulators that are sufficiently upstream and robust to be suitable for developing plants with optimized root systems for nutrient uptake [8].

4.3 Improving translocation (partitioning/remobilization)

Levels of fertilizer applications influence the total dry matter accumulation, thereby affecting the nutrient demand (uptake/utilization) [9]. Improved nutrient utilization efficiency from agrochemicals through PGPR and (or) AMF can contribute to the protection of water resources against agro-pollution and reduce the growing cost of fertilizers [10]. After inorganic phosphate (Pi) acquisition from rhizosphere, Pi should be efficiently transported to shoot for the requirement of plant growth by phosphate transporters (Pht1, Pht2, Pht3, and Pht4), which are located on the plasma membrane, plastidial membrane, mitochondrial membrane, and Golgi compartment, respectively [45]. In crops, a large fraction of the Pi present in vegetative organs is remobilized to the grain during the reproductive growth, and soil Pi availability at this stage has a relatively small effect on grain yield. Enhanced expression of high-affinity, plasma-membrane-bound Pi transporters in roots and a concomitantly increased P-up- take capacity were reported as a typical P-starvation response [46]. Moreover, enhanced metabolic activities of young tissues make them stronger sinks for the already absorbed P. Remobilization of stored P in the stem and older leaves to metabolically active sites may supplement the restricted P supply under P deficiency [29].

Another promising area for improvement of crop NUE is to enhance the efficiency of nutrient remobilization from senescing organs to young, developing organs, particularly immature leaves, and developing seeds [47]. The senescence process, that is, the dying-off of vegetative plant parts during seed maturation, is at the core of the nutrient use efficiency issue, as the nutrients need to be remobilized from these parts and translocated into the developing seed [48]. Maximizing the effectiveness of P-remobilization from senescing organs could make an important contribution to the development of crops that can tolerate Pi deficiency, because senescing organs of most “modern” crop varieties exhibit low P-remobilization efficiencies of <50% [30]. An integral understanding of P remobilization would facilitate development of effective biotechnological strategies to improve crop PUE, thereby reducing the rate of depletion of nonrenewable rock P reserves [30, 47]. Therefore, mobilization and redistribution of P from the old tissues to the young tissues will also contribute to high P use efficiency. Better distribution of nutrients in parts of plant (root, shoot, and grain) reflects their use efficiency [11].

4.4 Improving internal utilization

In the plant, uptake and utilization efficiency of nutrients are governed by different physiological mechanisms and their response to deficiency, tolerance, and toxicity of element(s) and climatic variables [49]. Efficient internal utilization of nutrient is generally attributed because of high photosynthetic activity per unit of nutrient (P) and more efficient P remobilization from older to young leaves [47]. Acid phosphatase contributes to the increased P utilization efficiency in bean through P remobilization from old leaves [50]. Therefore, improving higher total chlorophyll concentration [51], enhancing phosphorylase stimulation [52], and improving partitioning of carbon between glycolytic and pentose phosphate pathways [53] also provide an effective approach to improve phosphorus use efficiency and crop productivity simultaneously.

P-utilization efficient cultivars produce high yield per unit of absorbed P under P deficient conditions, since they have low internal P demand for normal metabolic activities and growth. Hence, they have low requirement for mineral P fertilizer inputs to produce reasonably high yield. Moreover, they remove less P from soil during growth and therefore the quantity of P removed along with the harvestable parts of the crop would obviously be less, consequently reducing the quantity of mineral P fertilizer inputs required for maintenance fertilization [54].

5. Optimization of agronomic practice

Agronomic practices can change soil physicochemical properties and biological characteristics. As a result, a number of agronomic practices have been proposed to enhance nutrient availability under diverse climatic conditions [55, 56]. The rhizosphere (root-soil interface) is the most important area for plant–soil-microorganism interactions and is the hub for controlling nutrient transformation and plant uptake [7]. This modification is paramount to increase nutrient availability and to minimize losses in surface runoff. Possible management strategies options for improving NUE through optimizing agronomic practice or rhizosphere modification [57] are the following:

5.1 Application of nutrient stewardship concept

The 4R Nutrient Stewardship framework promotes the application of nutrients using the right source (or product) at the right rate, right time, and right place. The framework was established to help convey how fertilizer application can be managed to ensure alignment with economic, social, and environmental goals [58]. Nutrient Stewardship defines the right source, rate, time, and place for fertilizer application as those producing the economic, social, and environmental outcomes desired by all stakeholders of the plant ecosystem (Figure 3). This 4R techniques applies (1) right rate—supplying growing crops with the right amount of nutrients for healthy growth and development based on experimentation under various environmental conditions; (2) right time—matching nutrient availability to with the timing of plant peak nutrient uptake and demand; (3) right placement adding nutrients to the soil at a place where crops can easily access them related to volume of roots.; (4) right source—applying the correct fertilizer and organic resources that provide growing crops with all nutrients required for good growth and maturity [58]. The 4R concept was established to help convey how fertilizer application can be managed to ensure alignment with economic, environmental, and social goals [22, 59].

Figure 3.

The 4R nutrient stewardship concept (adopted from [22, 59]).

Soil testing remains one of the most powerful tools available for determining the nutrient supplying capacity of the soil, but to be useful for making appropriate fertilizer recommendations good calibration data is also necessary [2]. As P is less mobile, less soluble, and highly prone to soil fixation; effectiveness of applied P depends on the properties of soil being fertilized, fertilizer itself, and time and method of its application [60]. To enhance phosphorus use efficiency (PUE) of applied P fertilizer, time and method of its application are critically important, because different P application methods differ in PUE [61]. In highly sandy soils, P may need to be managed like N, by splitting applications and applying small amounts at sowing and topdressing later in the crop growth cycle [62]. Studies of Jing et al. [63] suggested that localized supply of superphosphate combined with ammonium-N (NH₄⁺-N) significantly stimulated root proliferation, especially of fine roots, and thus improved maize growth in a calcareous soil. Further studies indicated that localized supply of P and NH₄⁺-N at both seeding and later growth stages increased maize yield by 8–10%, P uptake by 39–48%, and localized increases in root density and length of 50% [64]. Rehim et al. [65] also reported that the fixation of broadcasted P is much greater than the fertilizer applied in bands because of less contact with P fixing ingredients. At higher P application, the adsorption of P increased because the plants readily utilize only 8–33% of applied P in the first growing season and remaining portion remained fixed that consequently resulted in higher Olsen P. So, at higher P application rates, plants used smaller proportion of fertilizer P that resulted in low PUE [61].

In principle, N deficiency increases root growth, resulting in longer axial roots (primary roots, seminal roots, and nodal roots), and this helps maize roots to explore a larger soil volume and thus increases the spatial N availability [66]; however, long-term N deficiency stunts root growth due to insufficient N. But also, root elongation can be inhibited if the N supply is too high. Excessive application of N-P fertilizers may lead to high concentrations of soluble nutrients in the root zone, which can also restrict root growth and rhizosphere efficiency [67], even small amounts of P lost can be a cause of the adverse effects of eutrophication of surface waters. Therefore, judicious application of fertilizer best management practices (BMP) [22] that includes the right rate [68], right time [69], right source, right place, and balanced fertilization (4RB) is the best management practice for achieving optimum nutrient efficiency [2, 22].

5.2 Cereal-legume intercropping

Cereal-legume intercropping is a crop production system utilized to improve productivity and sustainability under diverse environmental conditions. It can also improve nutrient use efficiency and crop productivity [7]. Intermingling of maize and faba-bean roots increased N acquisition by both crop species by about 20% compared with complete or partial separation of the root systems. Further studies indicate that N₂ fixation can be improved by yield maximization in the intercropping system. The improved productivity observed in this production system has been associated with increased levels of available phosphorus (P) in the root rhizosphere. Hinsinger et al. [70] reported more stable yield, superior land resource utilization or conservation, and enhanced pest or weed control [71, 72, 73]. Furthermore, cereal-legume intercropping can also enhance the phosphatase enzyme activity and available P in the soil due to rhizosphere acidification by the legumes in the cropping system [74].

The possible mechanism that increases PUE in intercropping is the increased rhizosphere soil acid phosphatase (RS-AP_ase) activity observed in intercropping due to the fact that large amounts of acid phosphatase are known to be released from their roots into the root rhizosphere. The (RS-AP_ase) activity was significantly higher (26–46%) in the intercropping and occurred concomitant with a significant increase in available phosphorus (RS-P_available) in the rhizosphere on podzols in cool climate boreal ecosystem [75]. Another mechanism could be secreting H⁺ into the soil that acidifiies the rhizosphere [57, 76] and improves dissolution of phosphorus and then enhances P-availability [70]. Additional possible mechanism that improves of plant growth and P uptake in mixed planting was due to root interspecific complementation or facilitation. The complementarity between root morphological and physiological traits of neighboring plants underpins the interactive facilitation, which was the main underlying mechanism improving nutrient-use efficiency, particularly of P, in mixed cropping system [77, 78]. The complementary niches of maize and faba bean significantly reduce interspecific nutrient competition and thus improve nutrient-use efficiency [79]. The presence of maize increased the secretion of carboxylates from alfalfa roots, suggesting that the root interactions between maize and alfalfa are crucial for improving P-use efficiency and productivity in intercropping [80]. Subsequently, Sun et al. [76] reported that decreasing rhizosphere pH and increasing organic anion exudation played key roles in soil P mobilization of maize and alfalfa, with little contribution of acid phosphatase.

5.3 Effective microbial inoculation

The mycorrhizal symbiosis particularly, arbuscular mycorrhizal fungi (AMF), is arguably the most important symbiosis on earth [81]. AMF colonize the roots of many agriculturally important food and bioenergy crops form (approximately 80–90% of all known land plant species) [81] and could serve as “biofertilizers and bioprotectors” in environmentally sustainable agriculture [82]. In AMF associations, two pathways for plant P uptake exist: the direct pathway (P uptake by roots) and the AM fungal pathway [83]. AMF facilitates the uptake and transfer of mineral nutrients, such as phosphorus, nitrogen, sulfur, potassium, calcium, copper, and zinc, from the soil to their host plants by means of the extraradical mycelium extending from colonized roots into the soil [84]. The contribution of AMF to P uptake reaches up to 77% under low P supply compared with only 49% under high P supply [85]. Furthermore, the commercial inoculum Mycobiol, consisting of Glomus spp., Entrophospora colombiana, and Acaulospora mellea, enhanced P acquisition and plant growth in a pot experiment [86]. González and Walter [87] observed that Glomus aggregatum increased P uptake and biomass production of inoculated plants compared.

Various mechanisms have been suggested for the increase in the plant uptake of P. These include: exploration of larger soil volume; faster movement of P into mycorrhizal hyphae; and solubilization of soil phosphorus [88]. Exploration of larger soil volume by mycorrhizal plants is achieved by decreasing the distance that P ions must diffuse to plant roots and by increasing the surface area for absorption. Faster movement of P into mycorrhizal hyphae is achieved by increasing the affinity for P ions and by decreasing the threshold concentration required for absorption of P [88]. Solubilization of soil P is achieved by rhizospheric modifications through the release of organic acids, phosphatase enzymes, and some specialized metabolites such as siderophores [55].

The composition and amount of root exudates affect the composition of microbes in the rhizosphere and the structure of the rhizosphere microbiome, affecting plant growth and nutrient uptake [81]. For precision rhizosphere management, plant-microbe interactions must be finely tuned to improve P use efficiency by crops [57]. Figure 4 illustrates the main structural differences between AM (more for P absorption) and ectomycorrhizal (more for N and few for P absorption) associations of angiosperms or gymnosperms [81].

Figure 4.

Phosphorus acquisition efficiency related traits of wheat and barley roots affected by arbuscular mycorrhizal symbiosis in comparison to a non-colonized counterpart (adopted from [89]). (A) Representation of P depletion zone around the rhizosphere; (B) access to smaller soil pores by AM fungal hyphae; and (C) modulation of plant P transporters following colonization.

Among the soil bacterial communities, ectorhizospheric strains from Pseudomonas and Bacilli and endosymbiotic rhizobia have been described as effective phosphate solubilizers [90]. Phosphate-solubilizing bacteria (PSB) are also capable of making P available to plants from both inorganic sources and organic ones and increasing P-fertilizer-use efficiency by different mechanisms [91]. They are rhizobacteria that convert insoluble phosphates into soluble forms through acidification, chelation, exchange reactions, and the production of organic acids [92]. Therefore, combined application of AMF and P solubilizers [93] and N fixers are the best inoculants. AM fungi together with PSMs could be much more effective in supplementing soil P. Understanding AM-plant symbiosis, developing AM fungi that could be cultured in vitro, and developing P-solubilizing AM will help realize their potential as phosphate biofertilizer [94].

5.4 Regulating soil pH

Soil pH is one of the most important chemical properties influencing nutrient solubility and hence availability to plants. Large amount of P applied as fertilizer enters in to the immobile pools through precipitation reaction (fixation) with highly reactive Al³⁺ and Fe³⁺ in acidic and Ca²⁺ in calcareous or normal soils [94]. Acidic, highly weathered, iron (Fe)-rich soils rapidly bind phosphates at mineral surfaces, limiting access to plant roots. Furthermore, applied Pi (inorganic P) is quickly fixed into insoluble inorganic or organic forms due to its high reactivity and microbial action [95].

Soil pH markedly limits plant growth and P chemistry in soils through its effect on P adsorption and through interactions that affect precipitation of P into solid forms in soil [62]. Consequently, about 80–90% soil P becomes unavailable depending on soil composition and pH [96], 50–70% of the total applied conventional fertilizers are lost to the environment. This level of loss in agricultural nutrients not only leads to the loss of valuable resources but also causes the severe reduction of yield [97]. The pH of a calcareous soil is reduced by the presence of gypsum (CaSO₄·2H₂O) due to the concentration of Ca²⁺, which would be expected to decrease the sorption of P, if followed by leaching to removed much of the soluble Na⁺ and Ca²⁺ [98]. Thus, adjusting soil pH and base saturation are methods to reduce the amount of P that is bound by Al, Fe, and Ca, further reducing the effects of Al toxicity to plants, which can inhibit uptake, and use of P by the plant (Figure 5) [23, 99].

Figure 5.

Soil P availability as affected by soil pH (adopted from Havlin et al. 1999).

Lime acidic soil is widely used in agriculture to create and maintain a soil pH optimal for plant growth in acid soils. Lime reduces toxic effects of hydrogen, aluminum, and manganese, improves soil biological activities, cation exchange capacity (CEC), P, Ca, and Mg availability and soil structure, promotes N₂ fixation, stimulates nitrification, and decreases availability of K, Mn, Zn, Fe, boron (B), and Cu [11]. An increase in soil pH, as a result of liming, was due to an increase in hydroxide ions, which increases microbial activity and communities, hence, increasing decomposition of soil organic matter and release of Fe and Al [100]. The decrease in Al-P and Fe-P could be due to their precipitation as insoluble Al(OH)₃ and Fe(OH)₃ after increased addition of liming material [101]. In addition, Al and Fe oxides become more negatively charged with an increase in pH contributing to an increase in available P [102].

Liming, gypsum application, or mixing of both is an effective practice to improve pH, improve Ca content, and control Al toxicity. Lime has very low mobility in soil, and when surface applied, it does not reduce the acidity of subsurface soil horizons. Contrary to lime, gypsum (CaSO₄) has a greater downward movement, and when applied to the surface, it can still impact and reduce the acidity of the subsoil [4]. The pH of a calcareous soil is reduced by the presence of gypsum (CaSO₄·2H₂O) due to the concentration of Ca²⁺, which would be expected to decrease the sorption of P, if followed by leaching to removed much of the soluble Na⁺ and Ca²⁺. The uptake of nutrients by plants, content of nutrients in plants and in soil were substantially positively influenced by both the wood ash, especially by FGD gypsum [103]. Gypsum application can ameliorate saline-sodic soil, thereby increasing crop yield and NUE [104].

5.5 Application of advanced techniques

Apart from traditional methods, new techniques have been developed such as site-specific/real-time nitrogen management, slow release/controlled release fertilizer (SR/CRF), site-specific precision nutrient management, and urease/nitrification inhibitor. Those techniques play an important role in decreasing fertilizer loss and increasing NUE [105]. The remote sensing is quicker than the previous two methods, and it obtains continuous data rather than spot data, which is more advantageous. It is becoming the major means of obtaining data for precision farming. GIS (geographic information system) establishes the field management information system by processing, analyzing, and trimming the data of soil and crops [105]. Another approach to synchronize release of N from fertilizers with crop need is the use of N stabilizers and controlled release fertilizers. Nitrogen stabilizers (e.g., nitrapyrin, DCD [dicyandiamide], NBPT [n-butyl-thiophosphoric triamide]) inhibit nitrification or urease activity, thereby slowing the conversion of the fertilizer to nitrate. The most promising for widespread agricultural use are polymer-coated products, which can be designed to release nutrients in a controlled manner.

Agronomic management strategies such as precision P fertilization, polymer coated P-fertilizers, and recycling of P from domestic, agricultural, and industrial wastes can be helpful in improving P use at farm level [106]. Modern concepts for tactical N management should involve a combination of anticipatory (before planting) and responsive (during the growing season) decisions [9]. On soils with moderate P and K levels and little fixation, management must focus on balancing inputs and outputs at field and farm scales to maximize profit, avoid excessive accumulation, and minimize risk of P losses. Improving the internal, on-farm and field recycling is the most important K management issue worldwide. As for N, the primary determinants for RE_P and RE_K are the size of the crop sink, soil supply, soil characteristics, and fertilizer rate.

Control release fertilizers with polymer coatings are commonly applied to crops to increase efficiency of nutrients [96]. One way of improving the P availability to crop plant is by coating diammonium phosphate (DAP) with polymer that allows a steady but controlled discharge of phosphorus from the granules for crop plant uptake and improved P recovery percentage. Thus, by the use of polymer, availability of P to plant increased because it has high cation exchange capacity, which holds the divalent calcium (Ca⁺²) and trivalent cations iron and aluminum (Fe⁺³ and Al⁺³) and stop P fixation with these cations. Moreover, polymer absorbs water efficiently and holds more water and keeps P in available form that enhanced the plant growth and yield-contributing factors [97]. This is because polymer-coated diammonium phosphate (DAP) absorbs water many times of its original weight, which increases the availability of phosphorus for longer period of time [107] and creates a diffusion shell around the grain of DAP and directly reduces the fixation and precipitation by reducing the availability of calcium and magnesium (Ca⁺²/Mg⁺²) cations [108]. As the result of this mechanism, availability of phosphorus to plants increases and leads to more P uptake, and this uptake indirectly influences the other nutrient absorption by crop plants.

5.6 Use integrated soil nutrient management practice

Considering the wide variety of soil types, cropping patterns, and farmers’ resources, several management practices are adopted to reduce the magnitude of soil fertility degradation. Integrated Plant Nutrient Management System (IPNMS) is defined as the package of practices for the manipulation of the plant growth environment to supply essential nutrients to a crop in an adequate amount and proportion for optimum production without degrading the natural resources [3]. Many authors have reported that combining organic and inorganic P can improve and sustain crop yields in low fertility soils [109, 110, 111]. Best management practices (BMPs) such as use of fertilizer and amendment (lime), proper crop rotations, increases in organic matter content, and control of erosion, insects, diseases, and weeds can significantly improve crop yields and optimize nutrient use efficiency [11]. Integrated use of organic manures and fertilizers not only improves efficiency of crops but also significantly increases the availability of P [112, 113].

Organic amendment improves the structure and fertility of the soil by adding nutrients and organic matter and consequently promotes soil microbial biomass and activity. Blockage of P sorption sites by organic acids, as well as complexation of exchangeable Al and Fe in the soil, is potential cause of this mobilization [114]. Organic materials can reduce P fixation by masking the fixation sites on the soil colloids and by forming organic complexes or chelates with Al, Fe, and Mn ions, thereby improving P uptake efficiency of crop plants. Decomposition of organic matter produces organic anions that interact with soil to reduce P sorption via (1) complexation/competition for soil P binding sites such as Fe and Al oxyhydroxides or (2) increased soil P^H. Organic materials also increase agronomic efficiency by improving availability of P by promoting soil aggregation, increased soil P^H, microbial biomass, and parameters controlling soil-P-sorption [115]. The integration of biochar FYM, poultry manure, and inorganic P sources increases in PUE under both wheat and maize crops, and there is a concomitant increase in crop yields compared with the unamended soil [112, 113]. This increase in PUE with biochar addition could also be the result of the additional nutrients made available by biochar [112]. Similarly, FYM applications increase soil P bioavailability more than applications of triple supper phosphate that enhance P Uptake Efficiency. FYM is also a source of other nutrients used by crops via mineralization, which promotes root development and root area interception and thus increases nutrient uptake including P uptake [116].

Rotating a legume with a cereal can enhance P acquisition by cereals through indirect feedback interactions [117]. A legume crop modifies the rhizosphere through biological and chemical processes, thereby increasing P uptake by the following cereal crop. As reported by [77], legumes are able to mobilize P that is not initially available to cereal species, thereby improving the availability of P for the following crop. The biological processes include the promotion of symbiotic mutualists such as nitrogen-fixing rhizobacteria and mycorrhizal fungi, while the chemical processes are acidification of the rhizosphere and secretion of organic anions [79].

6. Conclusion

Achievement and maintenance of high nutrient use efficiency (NUE) together with high crop productivity have become a major challenge in both developed and developing countries with an increasing growing population, depletion of natural resources, and deteriorating environmental conditions. Improving nutrient use efficiency (NUE) in plants is vital to enhance the yield and quality of crops, reduce nutrient input cost and improve soil, water, and air quality [3]. Higher NUE by plants could reduce fertilizer input costs, decrease the rate of nutrient losses, and enhance crop yields. Improving crop nutrient use efficiency ideally requires an understanding of the whole system, from the macro (agro-ecosystem) to the molecular level.

The development of nutrient-efficient crop varieties that can grow and yield better with low supply is a key to improving crop production. A prerequisite for nutrient use efficiency for any germplasm will be the optimization of agronomic practice for any given environment and season. Judicious application of fertilizer that includes the right rate, right time, right source, right place, and balanced fertilization (4RB) is the best management practice for achieving optimum nutrient efficiency. By the coordination of the acquisition, root-to-shoot translocation, utilization, and remobilization of internal Pi can be achieved through genetic breeding. Selection and breeding nutrient efficient species or genotypes within a species are justified in terms of reduction in fertilizer input cost of crop production and also reduced risk of contamination of soil and water. Overall NUE in plant is a function of capacity of soil to supply adequate levels of nutrients and ability of plant to acquire, transport in roots and shoot, and remobilize to other parts of the plant. Improvement in NUE will ultimately come from integrating a range of different approaches to develop a more efficient farming system. Use of nutrient efficient crop species or genotypes within species in combination with other improved crop production practices offers the best option for meeting the future food requirements of expanding world populations. Modern tools and resources available to plant scientists and the agronomy and breeding communities should aid further improvements in NUE and hence crop production. Therefore, integrated strategy that seeks to increase phosphorus use efficiency and simultaneously seeks to recover unavoidable phosphorus losses. The nutrient inputs in the intensive farming system should be optimized to achieve both high crop productivity and high nutrient use efficiency through maximizing root/rhizosphere efficiency in nutrient mobilization and acquisition.

Acknowledgments

The authors are highly thankful to researchers whose findings are included directly or indirectly in preparing this manuscript.

Conflicts of interest

The authors declare no conflict of interest.

Funding

The authors received no direct funding for this research.

Data availability

All data generated are included in this article reference’s part.

Abbreviations

AMF	arbuscular mycorrhizal fungi
BMP	best management practice
DAP	diammonium phosphate
FYM	farm-yard manure
NUE	nutrient use efficiency
PACE	phosphorus acquisition efficiency
PSB	phosphate solubilizing bacteria
PUE	phosphorus use efficiency
PUTE	phosphorus utilization efficiency