Carlos Felipe dos Santos Cordeiro
Ciro Antonio Rosolem- 1Department of Agronomy, College of Agricultural Sciences, University of Western São Paulo, Presidente Prudente, São Paulo, Brazil
- 2São Paulo State University (UNESP), College of Agricultural Sciences, Department of Crop Science, Botucatu, São Paulo, Brazil
Root growth is one of the main strategies to improve phosphorus (P) uptake from soils, but both root growth and P movement to the roots are impaired by soil water shortage. Several studies have evaluated the effect of P availability on root growth, as well as the impact of root growth on drought tolerance, but there is still a lack of unity in this knowledge. Thus, the objective of this review article is to identify the primary P management strategies that can enhance root growth and P acquisition in crops during dry spells. This review synthesizes studies published from 1963 to 2025, with emphasis on field-based experiments conducted under rainfed or water-limited conditions. For this purpose, articles carried out in different parts of the world were reviewed. Based on these studies, we found that the main challenge to improving P acquisition by plants under water stress is to enhance P availability in the soil subsurface, which remains wetter for a longer period. Broadcast application of P has been a problem mainly in rainfed and water-restricted environments, and application of P in the sowing furrow is recommended in these environments. The use of cover crops, crop-livestock integration, crop rotation, liming, adjustment of optimum pH, and increase of C and humic substances in the soil are important techniques to improve the availability and mobility of P in the soil and consequently the root growth and P uptake in depth. Plants and cultivars with larger root systems and especially long and dense root hairs can improve drought tolerance and PUE. Growth-promoting microorganisms can help in drought tolerance through better hormonal balance and root growth, but there is still a need for new knowledge associated with P solubilization under field conditions. Future research should seek to evaluate the interactive effects of the use of microorganisms, root growth, and drought tolerance with field studies in different production systems.
Highlights
● Surface P broadcast limits root depth and increases crop vulnerability to drought.
● Localized P placement enhances root development and improves yield stability under water stress.
● Cover crops and rotations enrich subsoil P and promote deeper root exploration.
● Root traits and root hairs are key targets to boost P efficiency with minimal energy cost.
1 Introduction
Phosphorus (P) deficiency affects 70% of the world’s arable land, significantly limiting root growth and yield (Yue et al., 2023). Phosphorus has limited mobility in acidic soils, with inorganic P concentrations in soil solutions ranging from <0.6 to 11 μM (Lambers and Plaxton, 2015). Although organic P concentrations tend to be higher, it must be hydrolyzed before plant roots can absorb it (Lambers and Plaxton, 2015). The application of phosphate fertilizer can increase soil P availability; however, it can also jeopardize soil health, environmental quality, and even plant development, depending on factors such as the rate of application, region, soil type, and climate (Khan et al., 2010).
Phosphorus use efficiency (PUE) in agricultural systems is low, leading to fertilizer application in excess to maintain economic yields. This excess P becomes adsorbed onto soil colloids or precipitates, a phenomenon referred to as Legacy P (Withers et al., 2018). According to Menezes-Blackburn and Giles (2018), inorganic P stocks in the soil account for an average of 57%, while the monoester P pool makes up 33% of the total soil P. This indicates a potential for agronomic use of Legacy P in the soil. However, when the P concentration in the solution decreases, the net solubilization and desorption of stabilized soil P is very slow. This process varies among different soils, influenced by factors such as pH, mineralogy, and organic matter content (Barros and Comerford, 2005).
Agriculture is foreseen to remain the greatest global consumer of freshwater resources until 2050, although its share is projected to decline (Rosegrant et al., 2009). To address the growing impacts of water scarcity on the environment and to increase food, fiber, and energy production, it is crucial to conserve water and improve yields in both rainfed and irrigated agriculture (Rosegrant et al., 2009). Phosphorus is a vital nutrient that limits crop productivity (Khan et al., 2010) and can threaten groundwater quality in certain regions. Interestingly, it also plays a key role in enhancing drought tolerance in diverse plant species (Jin et al., 2005). Therefore, enhancing PUE poses a significant challenge (Paz-Ares et al., 2022).
Long-term drought can increase soil P availability, but it also limits P uptake due to reduced water availability, which eventually decreases PUE (Bi et al., 2023; Iqbal et al., 2023). If water deficits occur during a crop’s vegetative phase, PUE decreases even further (Ruiz et al., 2020). Introducing deep-rooted species into cropping systems not only enhances drought tolerance through improved soil exploration but also plays a vital role in carbon sequestration and soil carbon storage (Fisher et al., 1994; Kell, 2011; Bagnall et al., 2022).
Key strategies to enhance PUE include developing specialized root systems, increasing the exudation of organic acids, and enhancing the expression of transport genes, such as those responsible for citrate and malate transport. Additionally, larger root systems contribute to improved PUE. Utilizing plant species that can access soil-bound phosphorus associated with aluminum (Al), iron (Fe), and calcium (Ca) is also beneficial (Merlin et al., 2016; Paz-Ares et al., 2022; Lambers and Plaxton, 2015). The microbiome plays a significant role in enhancing PUE as well (Paz-Ares et al., 2022). Stabilized root exudates, when combined with phosphorus-solubilizing bacteria, can stimulate root growth and increase phosphorus concentrations in plant tissues, thereby optimizing the use of less-labile inorganic phosphorus sources, such as calcium phosphate. However, the impact on soil organic phosphorus forms such as phytin is limited (Pantigoso et al., 2023). Specific microbial groups have been associated with increased PUE, including phosphorus-solubilizing bacteria such as Bacillus and Pseudomonas, arbuscular mycorrhizal fungi, and plant growth–promoting rhizobacteria such as Azospirillum, which enhance P acquisition through the production of organic acids, rhizosphere acidification, hyphal soil exploration, and stimulation of root growth.
Several mechanisms have been proposed to explain how plants improve phosphorus (P) acquisition and use efficiency under water-limited conditions. These mechanisms include modifications in root system architecture (greater root length density and deeper rooting), enhanced development of root hairs, exudation of organic acids and phosphatases, up-regulation of high-affinity P transporters, associations with arbuscular mycorrhizal fungi and other plant growth–promoting microorganisms, as well as agronomic strategies such as localized P placement, soil pH correction, crop rotation, and the use of cover crops capable of mobilizing less labile P pools. Despite these advances, important knowledge gaps remain. There is still limited field-based evidence on the interactive effects of drought intensity, P availability, root traits, and microbial activity, particularly under contrasting soil textures and management systems. In addition, uncertainties persist regarding the long-term contribution of microorganisms to the mobilization of non-labile P forms, the energetic trade-offs associated with enhanced root growth, and the scalability of these strategies across different cropping systems and climates. Therefore, this review aims to integrate current knowledge on soil P dynamics, root and root hair traits, microbial interactions, and agronomic management practices to identify the most effective strategies for improving PUE under an uncertain climate. The literature reviewed was selected from high-impact international journals using databases such as Web of Science and Scopus, with keywords including “phosphorus use efficiency”, “root growth”, “root hairs”, “phosphorus placement”, “drought stress”, “soil phosphorus dynamics”, and “phosphorus-solubilizing microorganisms”. Priority was given to long-term field studies, multi-season experiments, and studies conducted under rainfed or water-limited conditions, allowing a comprehensive assessment of mechanisms, limitations, and future research directions.
2 Soil P dynamics
2.1 Availability of P in soil
Phosphorus in soil exists in both organic and inorganic forms (H2PO4- and HPO42-). The relative proportions of these forms depend mainly on soil properties and management practices, though in some cases, inorganic P can constitute up to 80% of the total P content (Pavinato and Rosolem, 2023). It is currently estimated that global soil P contents range from 400 to 1000 mg kg-1, of which only 1.0% to 2.5% is available to plants (Pan and Cai, 2023). This limited lability results primarily from P fixation following fertilizer applications over time, especially in acidic soils (Pavinato et al., 2020).
P availability to plants is closely linked to soil pH. Research suggests that optimal P uptake by plants occurs at pH between 4.0 and 6.0 (Barrow, 2017), though the literature also cites a pH range of 6.0 to 7.0 for maximizing soil P availability (Penn and Camberato, 2019). Under acidic conditions (pH < 5.5), P binds to Fe and Al oxides, while in alkaline conditions (pH > 7.0) P binds to Ca. Therefore, the optimal soil pH for P availability lies between 6.0 and 7.0 (Penn and Camberato, 2019).
Soil C and microbiota are also critical to improving P availability to plants. Addition of labile C to soil improves soil P availability by displacing non-labile P into soil microbial biomass (Jing et al., 2017). Mycorrhizal fungi recruit a specific soil microbiome from the rhizosphere and stimulate P turnover to increase phytate P utilization (Wang et al., 2023). P-solubilizing bacteria are important for converting adsorbed P to labile P forms (Li et al., 2023).
Crop rotation, adequate P rates, and sources improve soil P availability and crop yield (Gotz et al., 2025). Brachiarias have been reported to have a high capacity to acquire less labile P forms (Merlin et al., 2016), increasing inorganic (resin-extracted) and organic (NaHCO3- extracted) soil P (Merlin et al., 2013) that could be available to the successor crop (Pavinato et al., 2024). However, there is still a need for new studies related to the use of cover crops, increased soil C and microbial diversity, with greater efficiency and availability of P in different production systems. The use of legumes in rotation with grass has also been a strategy to improve P availability. It has been reported that the cultivation of velvet bean (Mucuna pruriens) in rotation with corn improves P availability and uptake by crops when compared to the corn/corn system (Pypers et al., 2007). This was mainly attributed to the reduction of the pH of the rhizosphere of legumes, thus solubilizing less labile forms of P. Legumes can also improve P mobilization by increasing acid phosphate activity and releasing organic acids, depending on the species, and improving PUE (Tang et al., 2021). Thus, intercropping grasses and legumes is a strategy to improve P uptake and crop productivity in P-scarce environments, due to greater soil enzymatic activity, P solubilization and availability (Eichler-Loebermann et al., 2021).
2.2 P movement in the soil profile
Phosphorus typically exhibits low mobility in soil due to its strong fixation with Al, Fe, and Ca. Factors such as fertilizer type, pH, soil texture, and moisture can influence P mobility, with greater mobility observed in acidic sandy soils due to lower adsorption with clay (Nascimento et al., 2018). P diffusion increased from 1.1 × 10–7 to 6.7 × 10–7 cm2 from a soil with 17% to 51% clay, assuming equal soil P availability (Olsen and Watanabe, 1963). The diffusive flux of the H2PO4– ion to the roots is close to zero in dry soils, and therefore, soil water has a direct effect on P transport to the roots. According to Costa et al. (2006), soil water can be more important than soil P availability in the diffusion of the nutrient to the roots.
Humic substances can also improve P mobility in the soil. Humic acid acts as a chelating agent, complexing clay charges, which reduces P adsorption and increases mobility (Wu et al., 2020). Thus, the use of organic fertilizers can not only increase P availability in the soil, but also mobility (Von Wandruszka, 2006). Thus, no-till farming, crop rotation, and cover crops can improve soil C, and humic substances (Cordeiro et al., 2022), increasing P availability in the subsurface (Zhang et al., 2022; Rebonatti et al., 2023). The crop-livestock integration system can also affect P mobility in the soil, due to the deposition of organic animal residues on the soil surface and incorporation of P through pasture root growth (Costa et al., 2014). Covering phosphate fertilizers with humic substances improves P soil diffusion, but the effect depends on soil water (Rosolem et al., 2023). However, this effect was observed only for short distances. Cover crops with deep roots also aid in the vertical integration of P in the soil (Franchini et al., 2004). It has been reported that the most effective approach to increase P availability in the soil profile is by applying P in seed furrows, as shown in Figure 1. Broadcasting P fertilizers tends to concentrate P near the soil surface, increasing its susceptibility to erosion, which accounts for approximately 50% of total P loss in agricultural systems (Alewell et al., 2020). Additionally, this surface concentration limits deep root growth, making crops more vulnerable to drought (Hansel et al., 2017). However, plants can incorporate P deep in the soil profile through root growth and decay, as shown by Marubayshi et al. (1994) for peanuts and Leite et al. (2024) for crop rotations.
Figure 1. Spatial distribution of Mehlich-1 extractable phosphorus (P, mg kg⁻¹) in the soil profile, assessed vertically down to 25 cm and horizontally up to 37.5 cm on each side of the maize seed row. The figure illustrates P gradients in relation to fertilizer placement at the row–interrow scale. Adapted with permission from “Spatial distribution of soil phosphorus fractions in a clayey Oxisol submitted to long-term phosphate fertilization strategies” by Oliveira et al. (2022), Geoderma, licensed under© 2022 Elsevier B.V. All rights reserved. Source: https://doi.org/10.1016/j.geoderma.2022.115847.
3 Root growth
A better development of the root system can mitigate abiotic stress on plants, such as drought and elevated temperature, in addition to reducing the water used in irrigated environments (Calleja-Cabrera et al., 2020). During periods of water deficit, the architecture of the root system undergoes morphological changes to increase its capacity to take up water, such as cell division, elongation, and differentiation at the root apex, resulting in longer and deeper roots with reduced branching angles, and improved water acquisition in the subsoil (Gupta et al., 2020). Another adaptive response to the inhomogeneous distribution of moisture throughout the soil is hydrotropism, in which roots grow toward zones with higher water content to optimize the architecture of the root system for water acquisition, a process that is coordinated by abscisic acid (Dietrich et al., 2017). However, there is still much work to be done to improve drought tolerance through root growth (Gupta et al., 2020).
The first step is to define the main characteristics of the roots associated with drought tolerance. Comas et al. (2013) reported that characteristics such as smaller diameter, greater length, and considerable root length density, especially at depths in the soil with available water, are fundamental. Another important point is that the rapid resumption of root growth after soil rewetting can improve plant productivity under temporary droughts. Additionally, it has been reported that adequate P fertilization has improved drought tolerance and soybean productivity, due to greater root growth (Jin et al., 2005; Hansel et al., 2017). However, in low soil P soils, the transport of the nutrient to the cotton root surface limited P uptake. In this case, an increase in root growth rate due to P fertilization did not compensate for the low P diffusion in the soil (Rosolem et al., 1999).
A better understanding of root systems can provide the grounds for a greater efficiency in the use of nutrients and water, in addition to increasing crop productivity, but there is still little information on the phenotyping of root systems, and great progress is needed in this area, especially at the field level, since most studies are carried out under controlled conditions (Atkinson et al., 2019). At the field level, it has been reported that there is a relationship between shoot and root growth and that this is dependent on the phenological phase of the crop (Mayaki et al., 1976). For soybeans, root length is twice the shoot up to the beginning of pod formation, but in the reproductive phase, the difference is only 1.4 times (Mayaki et al., 1976). About 60% of the root volume is in the first 0–15 cm layer of the soil, but soybean roots can reach depths of up to 1.6 m (Mayaki et al., 1976). In cotton, root growth rate is 2.6 times greater than the shoot growth up to the appearance of the first flower, with approximately 1.8 cm day-1, but after that the growth rate decreases (Oosterhuis, 1990). Similar results were also reported for maize (Shao et al., 2018) and rice (Beyrouty et al., 1988). Therefore, roots are the main sink of photo assimilates in crops up to the beginning of the reproductive phase.
3.1 Factors determining root growth
On a macroscale, root growth is strongly affected by soil texture, water availability and nutrient availability (Rellán-Álvarez et al., 2016). Soil texture directly affects root architecture but has little effect on total length (Ruger et al., 2023). This is because, as the percentage of sand and apparent density of the soil increases, the length of the main root reduces and increases the length of the lateral roots, that is, there is compensatory growth depending on the soil texture (Ruger et al., 2023). Furthermore, the size of soil particles determines the pore space between particles. As a result, sandy soils have a greater amount of pore spaces, which often facilitates root growth and water infiltration capacity, but they have a low water retention capacity compared to clay soils, which can expose crops to drought prematurely, in addition of limiting root growth due to water deficiency (Rellán-Álvarez et al., 2016).
Nutrient availability is another important factor that modulates root systems (Bello, 2021). P availability is perhaps one of the most important factors affecting root growth, which is coordinated by plant hormones such as auxins, ethylene, and cytokinins (Wittenmayer and Merbach, 2005). It has also been reported that under P deficiency conditions, plants tend to develop a shallow root system and high lateral rooting, as this facilitates P acquisition (Liu, 2021). Under conditions of sufficient P content in the soil, the localized supply of ammonium increases the branching of plant lateral roots due to acidification of the rhizosphere and greater accumulation of auxin in this plant tissue (Meier et al., 2020), and this may explain the best efficiency in phosphorus absorption in acidic soils when P is applied associated with NH4+ (Rosolem et al., 2022).
Under high nitrate availability, maize shows a tendency to increase the length and decrease the density of lateral roots, but when there is high availability of P, there is a reduction in the length of lateral roots and densification of the root system (Postma et al., 2014). A better P nutrition, in addition to improving maize root growth, also increases macronutrient uptake (Rosolem et al., 1994). It is important to mention that root growth is facilitated in P-rich soil patches, which is normally observed in the uppermost soil layer, due to the deposition of crop residues that release P and the application of fertilizers, that is, there is a greater concentration of the root system in the surface soil (Liu, 2021). However, for plants to be more tolerant to drought, root growth must be enhanced deeper in the soil profile (Smith et al., 2005; Kell, 2011; Comas et al., 2013; Madhu and Hatfield, 2013; Aslam et al., 2022a).
3.2 Root growth in the subsoil and availability of P
Root growth in the subsoil can be limited by soil acidity, high levels of aluminum, phosphorus and calcium deficiency, and soil compaction and temperature (Lynch and Wojciechowski, 2015). Regarding P, approximately 70% of the land surface and half of the agricultural land are P deficient (Lynch, 2011). Furthermore, P has low mobility in the soil, with a higher concentration in the surface layers of the soil (Lynch, 2011). P deficiency has been reported to limit root growth in cotton (Rosolem et al., 1999), rice (Okada et al., 2004), soybean (Cassman et al., 1980; He et al., 2019; Rosolem et al., 2022), maize (Zhang et al., 2016), wheat (Van der Bom et al., 2023), peanut (Cordeiro et al., 2024), among other crops. But P placement must also be taken into consideration, since the deep and localized application of P has improved root growth of some crops (Jing et al., 2010; Liu et al., 2022; Chen et al., 2022; Mumtahina et al., 2023), and water uptake below the depth of 20 cm under drought (Okada et al., 2004), which improves drought tolerance (Kang et al., 2014; Hansel et al., 2017). This is because when P is localized at depth, in addition to increasing the root volume where there is a greater concentration of P, the number of roots in the 40–50 cm layer also increases. Conversely, when P is broadcast on the soil surface, there is a tendency for the roots to concentrate only in this layer, and the volume of soil exported is smaller (Van der Bom et al., 2023). Therefore, the location of P in the soil is as important as the application rate to increase root growth in the soil profile.
3.3 Energy cost for root growth
It is important to highlight that there is an additional energetic cost for greater soil exploration by bigger root systems (Kell, 2011; Lynch, 2015), mainly for the formation of new roots, while the cost of maintaining roots is 10 times lower (Madhu and Hatfield (2013). This can impair crop yields because carbohydrates that would be used for the formation and filling of reproductive structures are now diverted for root formation (Kell, 2011; Lynch and Wojciechowski, 2015). Thus, while enhancing root growth improves drought tolerance, it can limit yields due to competition for carbohydrates within the plant (Caldwell, 1979; Kell, 2011). However, this does not seem to be true for forage grasses (Fisher et al., 1994). The challenge is to improve the performance of root systems without penalty for canopy growth and development (Calleja-Cabrera et al., 2020). There are some strategies plants use for this, such as the formation of root cortical aerenchyma, which results in programmed cell death, root etiolation, cortical senescence, and cortical cell size (Lynch and Wojciechowski, 2015). However, root hairs seem to be more promising since they have low energy costs for plants and improve P acquisition efficiency (to Bates and Lynch, 2000), in addition to having the potential to improve water use efficiency (Brown et al., 2012; Cai and Ahmed, 2022).
4 Root hairs
4.1 Knowing root hairs
Root hairs are structures that grow at the tips of young roots, increase the contact area between plant and soil (Datta et al., 2011), and improve the efficiency of P uptake when the content in the soil is low (Lambers, 2022). A plant can have up to 14 billion root hairs that provide 8 m2 of surface area in 1 L of soil (Datta et al., 2011). The formation, length, and volume of root hairs are determined by plant genetics, environmental conditions (soil humidity and temperature) and availability of nutrients in the soil, mainly phosphorus and nitrate - when these nutrients are deficient, greater hair formation occurs (Jungk, 2001; Datta et al., 2011).
Auxin is the main plant hormone that determines the location, initiation and growth of hairs, so plants with a lower rate of auxin production have less stimulation for the formation of these structures (Jones et al., 2009), as well as ethylene, which is more associated with the induction of formation than with the growth of root hairs (Zhang et al., 2003). The lifespan of a root hair during the vegetative phase of the crop is longer compared with the reproductive phase, possibly because during the reproductive phase the competition for carbohydrates is greater (Xiao et al., 2020), with a lifespan between 2 and 3 days (Fusseder, 1987; McElgunn and Harrison, 1969).
4.2 Root hairs and drought tolerance
High soil temperatures (<26°C) accelerate hair death, with the optimum soil temperature for hair growth being between 18°C and 26°C (McElgunn and Harrison, 1969). The availability of water is also important for maintaining root hairs, since during the soil drying process, root hairs shrink (Cai and Ahmed, 2022), in addition to accelerating death (Xiao et al., 2020). The occurrence of high temperatures and droughts often raises doubts about the importance of root hairs for improving drought tolerance.
Recently, Cai and Ahmed (2022) carried out a review on the importance of root hair for water uptake. The main conclusions were that only long barley hairs will contribute to greater drought tolerance and that there is a need for more studies in this field. However, Datta et al. (2011) reported the presence of water influx in root hairs. Zhang et al. (2023) demonstrated that under dry conditions, plants can increase their ability to take up water by increasing the number and length of root hairs. Therefore, the effects of root hairs on drought tolerance are apparently indirect. This is because root hairs are also of great importance for the exudation of organic acids, increasing plant/soil interactions, nutrient cycling and C sequestration (Holz et al., 2018). The greater exudation of organic compounds in plants with a greater volume of root hairs can improve drought tolerance due to greater hydrolytic enzymatic activity and decomposition of organic matter in the rhizosphere soil (Zhang et al., 2023). The presence of root hair also increases the formation of rhizosheaths, the soil that is strongly attached to the roots (Burak et al., 2021). This property of the rhizosphere reduces water depletion around the roots and weakens the drop in water potential towards the roots, thus favoring water absorption under drought (Carminati et al., 2010; Aslam et al., 2022b). Thus, the greater formation of rhizosheaths enhanced by root hairs can improve drought tolerance (Cheraghi et al., 2023).
Techniques that enhance the formation of root hairs are important. High soil P availability can reduce the length and density of root hairs (Ma et al., 2001; Zhang et al., 2003; Nestler and Wissuwa, 2016). This happens because when there is a high availability of phosphorus, ethylene synthesis is lower, and there is no stimulus for the formation of root hairs (Borch et al., 1999; Zhang et al., 2003). Although the critical level of P in the soil for good hair formation has not been established, it does not seem to be interesting to maintain soils with a high concentration of P (above the critical level for crops) in the arable layer, as this will limit hair growth. Roots, root growth in depth, P uptake, shoot P concentration, PUE, and drought tolerance (Figure 2; Brown et al., 2012; Li et al., 2014; Bello, 2021).
Figure 2. Root and root hair growth of peanut (Arachis hypogaea L.) as affected by water and P availability in the soil.
4.3 Root hairs and P acquisition
One of the main contributions of root hairs to plant nutrition is to improve PUE (Lambers et al., 2006; Brown et al., 2012; Li et al., 2014; Heuer et al., 2017). It is estimated that root hairs can contribute up to 50% of the P taken up by plants (Ruiz et al., 2020). Typically, species with greater volume and length of root hairs have greater efficiency in P uptake (Burak et al., 2021) and a lower response to fertilization with P-fertilizers (Lambers et al., 2006). This is variable within the same species with differences between cultivars (Krasilnikoff et al., 2003; Cordeiro et al., 2024). Furthermore, root hairs have been important for P acquisition when P deficiency is associated with drought (Klamer et al., 2019), with a positive correlation between root hairs and productivity under low P availability and drought (Mohammed et al., 2022). Additionally, root hairs enhance P acquisition at a minimal carbon cost, while mycorrhizae and root exudates also enhance P acquisition, but at a significant carbon cost (Lynch et al., 2005). Thus, root hairs are an important strategy for bringing less labile forms of P into production systems, reducing the use of mineral fertilizers, with low energy costs for plants (Krasilnikoff et al., 2003). Therefore, it is recommended to select genotypes with greater length and density of root hairs, with heritability of these characteristics – between 34 and 77% (Mohammed et al., 2022).
5 Microorganisms
5.1 P-solubilizing microorganisms
The use of phosphorus-solubilizing and growth-promoting microorganisms has been frequently used in modern agriculture (Hernandez et al., 2024). The main P-solubilizing organisms are bacteria, fungi, arbuscular mycorrhizae, and cyanobacteria, which are present in most soils around the world, mainly in the rhizosphere (Silva et al., 2023a). Bacteria are mainly represented by the genera Azospirillum, Bacillus, Pseudomonas, Nitrosomonas, Erwinia, Serratia, Rhizobium, Xanthomonas, Enterobacter and Pantoea. Fungi are separated into mycorrhizae (Rhizophagus irregularis, Glomus mossea, G. fasciculatum and Entrophospora colombiana) and non-mycorrhizae (Penicillium, Fusarium, Aspergillus, Alternaria, Helminthosporium, Arthrobotrys and Trichoderma) (Silva et al., 2023a). However, those that have shown greater efficiency in solubilizing P are Bacillus, Pseudomonas, Rhizobium, Aspergillus, Penicillium, and mycorrhizae (Fatima et al., 2022). This market has experienced exponential growth in recent years, reaching US$1.57 billion in 2018 with an annual growth rate close to 12% (Modor Intelligence, 2022) and approximately 16% are phosphorus solubilizing products, which promise to reduce the use of phosphate fertilizers.
One explanation for better efficiency in the use of P using P-solubilized microorganisms is that these bacteria are involved in numerous biochemical processes in the soil such as solubilization, mineralization, and temporary immobilization of P (Bargaz et al., 2021; Fatima et al., 2022), in addition to changing the pH of the rhizosphere (Yue et al., 2023). There are different mechanisms associated with these microorganisms, when it comes to the use of P bound to Al, Fe and Ca (inorganic P), microorganisms, when associated with plant roots, enhance the release of organic acids such as glucose, oxalic and citric acids, which can transform insoluble P into soluble P forms for plants (Xu et al., 2019). The organic phosphorus in the soil is mineralized mainly by enzymes such as phosphatase and phytase (Owen et al., 2015; Pantigoso et al., 2023). However, there is still a large gap in the knowledge regarding the rhizosphere-microorganisms-nutrient uptake interaction, as the specific mechanisms that govern the assembly of the plant microbiome are extremely complex and difficult to predict (Jacoby et al., 2017).
5.2 Efficiency of P solubilizers
Failures of these microorganisms have been reported in some cases, which may be associated with poor survival of fungi in the rhizosphere, competition from native microbial communities, physicochemical properties of soils, signaling compounds released by different plant genotypes, availability of inadequate nutrients in the rhizosphere to produce sufficient organic acids, variation in the persistence of P solubilizing activity, and genetic instability among inoculated strains (Khan et al., 2010). However, in most cases, increases in growth and productivity have been reported using these inputs, but it is still not known exactly what mechanisms resulted in yield gains (Vessey, 2003; Owen et al., 2015; Kudoyarova et al., 2017; Rawat et al., 2021), in addition to reducing the need for mineral fertilizer (Yahya et al., 2021). It has been reported that although these microorganisms increased crop growth and productivity, improved P uptake was not the main benefit (Freitas et al., 1997). However, recently is has been reported that the application of these inputs, when carried out correctly and associated with mineral fertilizers, has improved root growth and drought tolerance, but positive responses have been conditioned by several factors such as the cropping system, soil type, genotype and associations between microorganisms (Benmrid et al., 2023). Nevertheless, it is not known to date whether there is mobilization of non-labile P by these microorganisms. It has been reported that in most cases it is likely that the greater efficiency in P uptake with the use of these products is associated with a decrease in pH in the rhizosphere (Barrow and Lambers, 2022; Yue et al., 2023; Barrow, 2025), but this still needs to be further discussed since maximum P availability for plant uptake is at pH in the range of 6-7 (Penn and Camberato, 2019).
5.3 P-solubilizing microorganisms and root growth
Interestingly, in a meta-analysis with approximately 171 peer-reviewed publications, it was reported that most of the positive responses to biofertilizers occurred in a dry or tropical climate and rarely in an oceanic or continental climate (Schütz et al., 2018). This may be happening because there are numerous studies showing the positive effect of these microorganisms on root growth and adjustment in the hormonal balance of plants under water stress and has improved crop productivity in situations of water deficit (Leyval and Berthelin, 1989; Katiyar and Goel, 2003; Vessey, 2003; Mahanta et al., 2014; Yahya et al., 2021; Kudoyarova et al., 2017; Chen and Liu, 2019; Sheteiwy et al., 2021; Rawat et al., 2021; Aslam et al., 2022a; Cheto et al., 2023; Silva et al., 2023b; Janati et al., 2023; Yue et al., 2023). Also, the modulation of the root system through the use of bacteria is coordinated mainly by adjusting the auxin/cytokine ratio and ethylene level in plants and this has improved the efficiency in the use of P (Hernandez et al., 2024). Furthermore, greater auxin synthesis correlated with greater root growth and P content in plant tissue (Kudoyarova et al., 2017). Additionally, mycorrhizal fungi can improve soil structure, produce spores and hyphae networks in the rhizosphere to connect to plant roots, improving water acquisition, in addition to the osmotic regulation of plants (Aslam et al., 2022a). Thus, the main effect of P-solubilized microorganisms seems to be associated with enhancing root growth through better hormonal synthesis, and consequently drought tolerance and not just improving the use of less labile forms of P (Barrow, 2025), as has been reported until the moment.
The positioning of microorganisms must also be considered, as they will not be efficient under every situation. Mycorrhizae, for example, are more efficient in soils with a relatively low P content, but when the content is extremely low or high, these microorganisms have low efficiency (Lambers, 2022). The response of the use of biofertilizers on crop productivity is low when the P content in the soil is low, especially with the use of P-solubilizing and N-fixing bacteria (Schütz et al., 2018), that is, these products do not they must be substitutes for mineral fertilizers but used in combination. Additionally, there is still a need to select potent phosphate solubilizers with multifunctional plant growth-promoting characteristics and a longer shelf life (Rawat et al., 2021).
6 Agronomic practices
6.1 P application methods
One of the main agronomic practices when it comes to P management, root growth and drought tolerance is the method of application of this nutrient. Agronomically, it is known that most of the time the best method of applying P would be localized close to the seeds (Freiling et al., 2022), with the aim of improving efficiency in the use of P and crop productivity (Hansel et al., 2017) and avoid P losses through erosion (Williams et al., 2018; Carver et al., 2022), which can amount up to 9.6 kg ha-1 year-1 in some regions of the world (Alewell et al., 2020).
However, it is increasingly common to apply P before sowing crops, with the aim of accelerating sowing, without the need to supply fertilizers (Rosolem and Merlin, 2014). This is especially important in places with a large territorial extension, with more than one crop per year (soybean/corn, soybean/cotton, soybean/wheat), as delays in sowing lead to significant yield loss (Júnior and Sentelhas, 2019).
Although some long-term studies (17 years) show that, on average, there was no difference in yields between broadcast and localized P application (Nunes et al., 2020) - studies with supplementary irrigation as cited by Nunes et al. (2021). The same research group published studies showing that in a conventional tillage system (less water storage capacity) there is yield loss when P is broadcasted (Oliveira et al., 2019). One of the problems with broadcasting P is the lower drought tolerance of crops (Figure 3). This is because P has low mobility in the soil, and when applied to the surface it generates an availability gradient, with a high concentration on the surface and lower concentration in depth (Figure 2; Nunes et al., 2020). In this case the roots are concentrated on the surface of the soil (Zhao et al., 2023) due to the higher concentration of P in this region (Rosolem et al., 1999; Nunes et al., 2021), and have a lower capacity to take up water from deeper layers of the soil, leading to yield loss in dry years (Figure 3; Kang et al., 2014; Hansel et al., 2017).
Figure 3. Root growth, P availability, and drought tolerance in soybeans as affected by the way of P application.
We searched for articles published in high-impact international journals over the last 40 years. Only studies conducted under field conditions were selected, with at least two years of evaluation, which compares broadcast and localized P application (Table 1). There were 29 articles available from six different countries (China 11, USA 9, Brazil 4, Australia 2, Japan, Madagascar and Bangladesh 1). In these studies, 10 annual crops were evaluated. Yield was increased with localized P application in 68% of the cases compared with broadcast application, with an average increase of 24% (Table 1). However, when there was a drought, the yield increase with localized P compared with broadcasting was observed in 90% of the cases (17% increase in productivity). In 15 of the 29 studies, root growth of crops was evaluated, and only in two cases did localized application does not increase root growth in depth, compared with broadcast application (Table 1).
Table 1. Effect of the method of P application on yield, root growth and drought tolerance.
Despite previous reports that the preferred form of P application for soybeans would be broadcast (Freiling et al., 2022), in our survey, we were unable to reach this conclusion. Additionally, even though yield losses with broadcast P application are observed more frequently in sandy soils with low initial P content, this is not a rule, because losses have also been reported in some clay soils with adequate P content (Table 1). In the coming years, science should focus on other localized P application strategies to improve P distribution in the soil profile, root growth in depth, and avoid losses due to erosion.
6.2 Cover crops and crops with high PUE
Cover crops and species such as sorghum and peanuts are more efficient in solubilizing less labile forms of P, and this is mainly associated with roots. Roots that release large amounts of P-solubilizing carboxylates can access some of this adsorbed P (Lambers and Plaxton, 2015). Almeida et al. (2020) reported that grasses of the genus Urochloa exhibited a high exudation rate of organic acids such as citrate and oxalate under low P availability, resulting in greater PUE. This is due to the solubilization of forms of P associated with Al and Fe, for example (Merlin et al., 2016; Almeida et al., 2018a). Rosolem and Merlin (2014) reported a reduction in soil P-Ca when Congo grass was cultivated in different soils. It was found that grasses such as ruzigrass, palisade grass and Guinea grass remobilized soil P from recalcitrant forms, but the change observed in P desorption kinetics did not directly explain the observed variation in P bioavailability to soybean (Almeida et al., 2018b). Ruzigrass has been reported to reduce the concentration of phytase-labile phosphorus and myo-inositol hexakisphosphate in soil treated with phosphorus (Almeida et al., 2018c). Other economically important crops, such as crambe (Crambe abyssinica), sorghum, and peanuts, are able to mobilize low-solubility forms of phosphorus (Janegitz et al., 2017). However, as noted by Almeida et al. (2019), phosphorus supply to the soil solution decreased after the introduction of ruzigrass. This was due to slower phosphorus desorption, which reduced soil phosphorus availability for soybean crops by limiting the mobility and resupply of phosphorus from the solid phase into the soil solution. As a result, there remains a significant knowledge gap regarding how phosphorus is cycled within the system and the timing and mechanisms of its availability.
In addition to increasing the labile forms of P in the soil (Rodrigues et al., 2021), cover crops also have the capacity to carry out biological incorporation of P in deeper layers of the soil, through the cycle of root growth and death (Franchini et al., 2004). Therefore, the use of cover crops associated with no-till can be a good option to incorporate P into the soil and promote root growth of the succeeding crop. Cover crops in the off-season also increase the soil’s C stock and humic substances (Cordeiro et al., 2022). This is important for increasing soil water storage capacity (Bagnall et al., 2022) in addition to plant root growth (García et al., 2019), improving drought tolerance. Therefore, the inclusion of these crops in production systems is essential to improve efficiency in the use of P and drought tolerance.
Besides P incorporation in the soil profile by the roots, with the decomposition of plant residues from some species left on the soil surface and rains, P can be carried to soil deeper layers. For instance, pearl millet residue was shown to increase inorganic, while black oats and sorghum increased organic P down to the depth of 30–45 cm (Correa et al., 2004). Pavinato et al. (2008) applied aqueous extracts of black oat (Avena strigosa), radish (Raphanus sativus), corn (Zea mays), millet (Pennisetum glaucum), soybean (Glycine max), and sorghum (Sorghum bicolor) associated with P fertilization. After seven days, soil samples were taken from soil layers at various depths. Plant extracts led to an accumulation of inorganic phosphorus in labile and moderately labile fractions, mainly in the soil surface layer (0–5 cm). Radish, with a higher amount of malic acid and higher P content than other species, was the most efficient in increasing soil P availability. After 14 years of crop rotations under no-till, the use of cover crops such as sorghum, pearl millet, and Sunn hemp, labile inorganic P labile was higher to the depths of 0.40 – 0.60 m, and the systems using cover crops recovered 100% of the P applied to soybean (Rigon et al, 2024). In sandy soil, the use of tropical grasses in the soybean off-season increased the availability of labile P in the 10–20 cm layer compared to systems without cover crops (soybean/corn) (Froio et al., 2025).
6.3 Soil correction
Liming is essential for improving P uptake efficiency in acidic soil environments (Qaswar et al., 2020). This must be carried out with the aim of keeping the pH in the appropriate range and providing Ca and Mg within adequate concentrations for each crop, in addition to neutralizing Al (Qaswar et al., 2020) in the soil profile to assure root growth in depth (Souza et al., 2023). This will improve root growth, P uptake, drought tolerance, and crop yield.
6.4 Select species and genotypes with greater root growth and PUE
In the past, genetic improvement strategies focused on the plant canopy to select drought-tolerant species, looking at characteristics such as photosynthesis, but in recent decades greater importance has been given to root growth and good results have been obtained (Lopes et al., 2011). However, there are still important bottlenecks, as improving the allocation of biomass and crop yield simultaneously is still a challenge (Mathew et al., 2018). Therefore, it is important to have a more comprehensive view at this point, focusing on root hairs and efficiency in the use of nutrients, since the energy expenditure of root hairs is low and will have little impact on the allocation of C in reproductive structures (Krasilnikoff et al., 2003). Thus, the objective should be to select plants that are more efficient in using water and nutrients in combination.
Recent field studies reinforce this concept by showing that genotypes combining greater root growth in depth with higher nutrient use efficiency are better adapted to water-limited environments. In peanut grown in sandy tropical soils, late-maturing cultivars with larger and more plastic root systems exhibited higher yield stability and phosphorus uptake under drought, even at moderate soil P availability, highlighting the importance of selecting genotypes that efficiently integrate root growth, P use efficiency, and drought tolerance (Cordeiro et al., 2025).
7 Perspectives
Several adaptive mechanisms were developed by plants to enhance P acquisition, including modifications to root architecture and morphology, up-regulation of high-affinity P transporters, mycorrhizal associations, release of phosphatases and organic acids capable of mobilizing less labile P, among others (Lynch, 2011). Furthermore, it has been reported that enhanced P utilization efficiency could be achieved by optimal partitioning of cellular P and distributing P effectively between tissues (Han et al., 2022). However, soil parameters largely determine how much P roots can acquire from P-impoverished soil, and the kinetic properties of P transporters are less important.
Therefore, the biggest challenge to improving PUE in agricultural systems is related to P transport to the roots, mainly when water availability is low. To achieve this, there are some strategies (i) applying P-fertilizer close to the roots, (ii) using plants and cultivars with greater root volume that can explore deeper soil layers where there is greater water availability, (iii) using species with greater capacity to utilize less labile forms of P, (iv) crop rotation and intercropping that will benefit soil physics, chemistry, and biology, thus improving root growth, and (v) adjusting the optimum pH to improve P availability. P application close to the roots or the use of enhanced fertilizers would have a limited effect when the plant is going through a dry spell, because the first soil layer is the first to dry. This would be the case of adjusting the pH in the arable layer. Other management strategies, such as the use of growth-promoting microorganisms and P solubilizers, although promising, have been strongly argued (Barrow, 2025) and would not be effective if the arable layer dries out. We conclude that a combination of strategies (ii) to (vi) would be the best way to enhance PUE under an uncertain climate. New studies should focus on the interactive effects between drought, P availability, and the use of diverse cover crop species to improve water and PUE.
Author contributions
CC: Project administration, Writing – review & editing, Writing – original draft, Visualization, Formal analysis, Methodology, Conceptualization, Supervision, Validation, Data curation, Resources, Investigation. CR: Project administration, Visualization, Writing – review & editing, Conceptualization, Writing – original draft, Resources.
Funding
The author(s) declared that financial support was received for this work and/or its publication. The authors acknowledge the financial support provided by the São Paulo Research Foundation (FAPESP) through PhD scholarships awarded to the first author (Grants #2020/14810-8 and #2023/06072-5).
Conflict of interest
The authors declared that this work was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
The author CR declared that they were an editorial board member of Frontiers, at the time of submission. This had no impact on the peer review process and the final decision.
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Keywords: drought, fertilization method, P solubilizing crops, P transport, root growth
Citation: Cordeiro CFdS and Rosolem CA (2026) Management strategies to improve phosphorus use efficiency under an uncertain climate: a review. Front. Agron. 7:1630934. doi: 10.3389/fagro.2025.1630934
Received: 19 May 2025; Accepted: 29 December 2025; Revised: 24 December 2025;
Published: 04 February 2026.
Edited by:
Davey Jones, Bangor University, United KingdomReviewed by:
Vlad Stoian, University of Agricultural Sciences and Veterinary Medicine of Cluj-Napoca, RomaniaQamar Sarfaraz, Lasbela University of Agriculture, Water and Marine Sciences, Pakistan
Copyright © 2026 Cordeiro and Rosolem. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Carlos Felipe dos Santos Cordeiro, Y2FybG9zY29yZGVpcm9AdW5vZXN0ZS5icg==