Introduction

Phosphorous (P) is unarguably one of the most important macronutrients, next to nitrogen, of all life forms on earth. It is an important constituent of macromolecules such as nucleic acids, sugar phosphates and phospholipids. P is also essential for the growth of new tissues and cell division in plants. P contributes to about 0.2% of the total dry weight of plants (Sulieman and Tran 2017). It is also indispensable to numerous vital metabolic and signaling processes such as photosynthesis, macromolecular interactions, energy transfer reactions, respiration, signal transduction (Khan et al. 2010), and nitrogen fixation (Kouas and Labidi, 2005). Paucity of P leads to inhibited photosynthesis. P is taken by the roots mainly in its inorganic forms (Bieleski 1973). Soils around the globe vary greatly from very high to very low in terms of the spatial distribution of P (https://www.nrcs.usda.gov/wps/portal/nrcs/detail/soils/use/worldsoils/?cid=nrcs142p205401 4). MacDonald et al. (2011) has suggested that the soils in the majority of global agrosystems (~ 70%) is rich in P. Despite this, only a small percentage of soil P is often available to plants. A large fraction, amounting up to 80%, of total soil P is available in its organic form, especially as phytic acid (inositol hexaphosphate) (Anderson 1980; Alewell et al. 2020). According to an estimation, about half of the agricultural soils worldwide are deficient in P (Lynch 2011). Such deficiency in soils is either because of inadequate P replenishment into agrosystems (more likely in developing countries with limited access to fertilizers) or due to its fixation, which renders soil P unavailable to plants (Heuer et al. 2017). Thus, soil P may be copious in the soils of some regions, but its unrestricted availability to plants is not guaranteed. Therefore, chemical Pi-fertilizers are routinely applied to replenish the inorganic and bioavailable P deficiency in agricultural systems (Herrera-Estrella and López-Arredondo, 2016).

Due to the slow diffusion rate of P (10−12 to 10−15 m2s−1), its uptake by plants at high rates creates a depletion zone around the roots (Schachtman et al. 1998). Such Pi-depletion in the proximity of roots is often slowly alleviated. Therefore, Pi deficiency often leads to compromised plant growth (Lόpez-Bucio et al. 2000; Bindraban et al. 2020). The bioavailability of P is strongly affected by soil pH as mildly acidic soil pH favours its maximum solubility and plant availability. The formation of iron (Fe) and aluminum (Al) phosphate minerals such as strengite (FePO4.2H2O) and variscite (AlPO4.2H2O), respectively, reduce its bioavailability in strongly acidic soil (Richardson 2001). Likewise, in the alkaline pH (around 8), soil Pi reacts with calcium (Ca) and form insoluble Ca-Pi complexes (Haynes 1982; Wang and Nancollas, 2008; Hopkins and Ellsworth, 2005). Besides its fixation in the soils, P loss from farms due to leaching, erosion, and runoff also challenges its availability in the agro systems. Soil erosion is considered one of the primary contributors to such loss and is projected to critically challenge global P availability in agriculture systems in the future (Alewell et al. 2020; Simpson et al., 2011).

The global demand for Pi-fertilizers reached to approximately 21 million tons in 2015 (Bindraban et al. 2020). This is estimated to further increase in the future to 22–27 million tons per year for croplands. In terms of grasslands, an additional requirement of 4–12 million tons of P is projected (Mogollón et al. 2018). To meet the increasing demand, worldwide production of Pi-fertilizer has also increased to 50 million tonnes in 2020 (http://www.fao.org/faostat/en/#data/RFN) (Fig. 1A). Although applying chemical Pi-fertilizers is integral to maintaining soil P fertility, their injudicious use in agricultural systems is known to affect soil health and crop growth, especially by disrupting the composition and function of soil microorganisms. For example, up to five-fold more Pi-fertilizer is applied to highly P-sorbing weathered and tropical soils (Simpson et al. 2011). Excessive Pi-fertilizers may reduce the microorganism's biodiversity that may become critical to crop health. Further, in the case of arbuscular mycorrhizal fungi (AMF)-colonized plants, increased diversion of host carbon to the mycobiont may affect plants' produce (Buwalda and Goh, 1982; Jakobsen et al. 2005; Kaminsky et al. 2019; Liu et al. 2018a, b). Because of these reasons, scientific and technological interventions to either cut down on the overall Pi-usage in agriculture systems or reclaim Pi from waste become essential for its long-term management. Improving the agronomic efficiency (defined as the increase in grain yield per unit of applied fertilizer) of mineral fertilizers, that falls between 20–30% for the currently used chemical Pi-fertilizers (Syers et al. 2008; Van de Wiel et al., 2016), wo uld also contribute in prolonging the availability of this natural reserves. This review first outlines the current knowledge on the interrelationship between P (in Pi-fertilizers) and agricultural systems. We summarize the benefits as well as ecological implications associated with intensively fertilized agrosystems. Plant adaptive strategies to Pi deficiency and the role of microbial associations in improving Pi uptake by roots is discussed. Solutions to minimize the adverse effects associated with intensive fertilization in agriculture are also argued. Due to the extensive coverage of the molecular events underlying plant phosphorus responses and the cellular Pi signalling pathways in several recently published excellent review articles (Ham et al. 2018; Crombez et al. 2019; Guan et al. 2021; Wang et al. 2021a, b; Cho et al. 2021), we have avoided an in-depth coverage of these topics in this article.

Fig. 1
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Source: Data from 1992–2020 was obtained from the Food and Agriculture organization website. b Annual subsidy outgo for P&K fertilizers in India. Source: Government of India Ministry of Chemicals and Fertilizers for a period from 2005 to 2020

a Global production of Pi-fertilizers.

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Global phosphorus reserves are finite

P-reserves are a non-renewable resource that is asymmetrically distributed globally. Three countries, including Morocco and Western Sahara (71%), China (4.8%), and Algeria (3%), together hold most of the global natural rock phosphorous (RP) reserves (Survey USG 2020). The majority of the developing countries lack large natural indigenous P-reserves and meet their demand by importing RPs or finished fertilizers. In past decades, the production and demand for Pi-fertilizers has steadily increased (Fig. 1A). Numerous statistical analyses predict that the demand for Pi would further increase and reach its peak by 2030 (Cordell et al. 2009). Although there is no consensus on the exact time of the complete depletion of RPs, P-reserves are anticipated to exhaust in the next few hundred years (Gilbert 2009; Sattari et al. 2016; Ockenden et al. 2017). Thus, a potential P crisis is imminent in the recent future that would challenge the sustainability of agriculture.

Environmental consequences associated with intensive fertilization

Most chemical Pi-fertilizers are synthetic and are primarily obtained from RP extraction. RPs generally contain two principal phosphorous-containing minerals, fluorapatite (Ca5(PO4)3F) and hydroxyapatite (Ca5(PO4)3OH). Following the treatment with sulphuric and phosphoric acids, water-soluble Pi salts of these minerals are produced. Some of the major chemical Pi-fertilizers are; Ca and Al phosphates (MAP, MCP, DAP), monopotassium phosphate, and triple superphosphate (Hedley and McLaughlin, 2005). Du ring the production of chemical Pi-fertilizers, disposal of a waste by-product, phosphogypsum, has always been a concern to the environment. The fertilizers industry is known to contribute to the enhanced levels of radionuclides such as Uranium (238U), Radium (226Ra), and Thorium (232Th) in the environment (Sahu et al. 2014; Casacuberta and Masqué, 2011; da Conceição et al. 2012). PR deposits often contain heavy metals such as Cadmium (Cd). Applying Cd-contaminated fertilizers to croplands may affect soil fertility; therefore, many countries have set tolerance limits for heavy metal additions to the soils (Mortvedt, 1996). Du e to its toxic effects, Cd once entered into the food chain via plants, may pose a serious threat to human health. Cd concentration in the vegetable crops follows a linear correlation with its concentration in the soils and increases in the edible plant parts with its increasing amount in the rhizosphere (Huang et al. 2004; Othman 2007).

P security is indispensable to sustainable agriculture

Overreliance of countries on the foreign RP reserves is critical as any volatile geopolitical or economic crisis in the biggest RP supplier countries may compromise the supply of P to the importing nations (Jasinski 2011). A good example of such apprehension becoming reality is the global economic crisis of 2008. As a consequence of the financial meltdown, the prices of international Pi spiked from $50 per tonne to $430 per tonne (Jones et al. 2020). In such a scenario, countries such as India, primarily dependent on imported P products, were reported to be among the most affected nations due to their severe national shortage (Cordell et al. 2009; Elser and Bennett, 2011; Alewell et al., 2020). Further, the cost of RPs has significantly increased to $700 per ton in 2015 (Amundson et al. 2015). In India, any sudden fluctuation or sharp increase in RP prices is generally met by raising the fertilizers subsidy. It is reported that the Department of Fertilizers, the Government of India approved Rs. 26,335/- crore in 2019–2020, as the subsidy outgo, to provide cheaper P and K-fertilizers to farmers. This subsidy outgo has remained above Rs. 20,000/- crores in the last few years (Fig. 1B) (https://fert.nic.in/sites/default/files/2020-09/Annual-Report-2019-20.pdf).

Phosphate starvation response and adaptive strategies in plants

The Pi absorbed by roots from the soils are maily available in its orthophosphate forms such as H2PO4− or HPO42− (Mardamootoo et al. 2021). There are two primary P sources in the soils, (i) the native P and (ii) externally applied P, as organic or inorganic complexes. The bioavailability of Pi is generally limited in the soils due to its rapid fixation with cations such as Ca, Al, and Fe (Kochian et al. 2004; McLaughlin et al. 2011). These insoluble complexes together with the organic P pools (mainly the decomposed parts of the living organisms) make it poorly mobile in the soils (McLaughlin et al. 2011). To cope with Pi limitations, plants have acquired several adaptive strategies, collectively called Pi starvation responses (PSRs). These adaptive measures are employed to improve Pi uptake and internal mobilization for its better access to plants (Theodorou et al. 1993, Raghothama 1999; Zhang et al. 2014a, b).

Reprogramming of root system architecture

PSRs are classified into local and systemic responses (for detailed information on sensing and signaling of Pi starvation, please refer to recent review articles by Chien et al. 2018 and Ham et al. 2018). The profound structural modifications in plants under Pi deficiency unarguably occur in the root system architecture (RSA), a localized PSR (Williamson et al. 2001; Peret et al. 2014). Modifications in root system are triggered by local alterations in external Pi and sensed by the root tip under depleted Pi conditions (Svistoonoff et al. 2007). As plants assimilate Pi primarily via roots, the reprogramming of RSA under Pi deficiency is advantageous to improve nutrients foraging. Altered primary root length, increased lateral roots, and longer and denser root hairs are some of the well-studied morphological changes observed in the roots of Pi-deficient plants (Bates and Lynch, 1996; Ma et al. 2001; Yan et al. 2004). Formation of cluster roots and a decrease of root angles to a shallower position also occur in Pi-deprived plants(Borch et al. 1999; Dinkelaker et al. 1995; Kim et al. 2008). The development and functioning of cluster roots in white lupin and the Proteaceae family members is a well-studied strategy by plants to maximize Pi uptake from its enriched patches in the soils (Lambers and Finnegan, 2011; Lambers et al., 2013; Cheng et al. 2011; Skene and James, 2000). Si nce cluster roots in Proteaceae members are more prominent in the top layers of the soils, secretion of organic acids strategy is preferred over the P scavenging through root extension to mobilize sparingly available Pi (Rath et al. 2010). The decreased growth angle of basal roots is also considered an effective strategy to maximize Pi-acquisition from the top layers of the soil in several plant species (Bonser et al. 1996; Hodge et al. 2009). Modification of RSA is coordinated by the coaction of multiple plant hormones such as auxin, ethylene, cytokinin and strigolactones (Cheng et al. 2013; Crombez et al. 2019; Giri et al. 2018; Ruzicka et al. 2007; Muller et al. 2008). Recently, Song et al. (2016) have implicated ETHYLENE-INSENSITIVE3 (EIN3), a key transcriptional regulator of ethylene signaling and response, in the promotion of root hair growth under Pi depleted conditions. Similarly, in two separate studies by Giri et al. (2018) and Bhosale et al. (2018), a signalling module involving auxin synthesis, auxin transport and transcriptional regulators controlling low Pi promoted root hair growth in Arabidopsis has been revealed. Strigolactone or jasmonate have also been implicated in the Pi-related lateral root formation, although the underlying molecular mechanisms remains to be deciphered (Crombez et al. 2019; Sun et al. 2014; Raya-González et al. 2012). Although RSA modification is a common adaptive response in plants subjected to Pi deficiency, comparison of the low Pi-induced RSA in Arabidopsis and several other crop germplasms indicates that such response is genetically determined and is highly species-specific (Bhosale et al. 2018; Giri et al. 2018; Niu et al. 2013; Van de Wiel et al., 2016; Camacho-Cristóbal et al., 2008; Devaiah et al. 2007).

Metabolic strategies for Pi mineralization in the rhizosphere

Secretion of organic acids, protons, phosphatases, or ribonucleases by roots in the rhizosphere is an efficient mechanism adopted by plants to improve Pi-acquisition from the organic P and insoluble-Pi mineral complexes in the soils (Singh and Pandey, 2003; Heuer et al. 2017; Dissanayaka et al. 2021) (Fig. 2). It is a localized PSR that helps mobilize and enhance the bioavailability of the available Pi in the soils (Hinsinger 2001). Releasing protons or organic acids by Pi-deficient roots causes acidification of the rhizosphere. Consequent mineralization of insoluble Pi-complexes or organic P compounds results in the release of Pi in the rhizosphere. Root exudation of carboxylates such as citrate, malate, and oxalate mobilizes Pi from Al, Fe, or Ca complexes through chelation and ligand exchanges in the rhizosphere (Shen et al. 2011). In this context, the role of malate not only in the mineralization of soil bound P but also in controlling RSA under Pi depletion is well-studied. Mora-Macías et al. (2017) through characterization of two low-Pi insensitive Arabidopsis mutants (lpi5 and lpi6) revealed existence of a regulatory module involving SENSITIVE TO PROTON RHIZOTOXICITY (STOP1) and ALUMINUM ACTIVATED MALATE TRANSPORTER 1 (ALMT1) in controlling malate efflux in the root apex. Such malate efflux leads to the aggregation of Fe3+ ions in the apoplast, which blocks the symplastic channels due to callose deposition. The closing of symplastic channels eventually impairs the communication of root apical meristem (RAM) with the neighbouring cells, leading to seizure of cell proliferation and root meristematic activity. Overall the authors demonstrated that malate-dependent Fe accumulation regulates RSA reprogramming in Pi-starved Arabidopsis seedlings (Mora-Macías et al., 2017). The role of ALMT1 transporters in conferring plants tolerance to Al3+ is also well investigated. In acid soils, Al3+ toxicity inhibits root growth, leading to inadequate soil exploration capacity of such roots for nutrients uptake (Delhaize et al., 2012). Be cause Al3+ activates ALMT1 transporter genes, the secreted malate can solubilize complexed soil Pi from Al-P complexes in the acidic soils. Consistent with the proposed roles of ALMT1 genes in Al3+ toxicity and Pi starvation, barley lines expressing an ALMT1 gene from wheat exhibited improved Al3+ tolerance and Pi uptake when grown in acidic soil (Delhaize et al. 2009). Zhang et al. (2020) have further demonstrated a similar interrelationship between Pi and Fe. A low Pi supply promoted organic acids exudation and simultaneously enhanced Fe absorption during its deficiency in apples. Another critical strategy to improve Pi-mineralization is the secretion of phosphatases or phytases by Pi-starved roots. Their release mobilizes Pi from the organic phosphate complexes through enzyme-catalyzed hydrolysis (Shen et al. 2011). A large body of evidence has demonstrated the induction of numerous phosphatases encoding genes in many plant species under Pi deficiency (Baldwin et al. 2008; Del Vecchio et al. 2014; Gao et al. 2017; Mehra et al. 2017; Srivastava et al. 2020). Several purple acid phosphatases (PAPs) and haloacid halogenases have been implicated to increase PUE and PAE in plants. A summary of such selected studies is provided in Table 1.

Fig. 2
figure 2

Summary of the key challenges associated with intensive Pi- fertilization and Pi starvation responses in plants. The strategies adopted by plants under low Pi to mitigate its deficiency are also highlighted. Plant response at morpho-physiological, biochemical and molecular levels related to Pi uptake (PHTs and HATs), homeostasis, and internal mobilization in plants are listed in the boxes. Role of microbes in mobilizing Pi from organic P pool or insoluble mineral P-complexes in the rhizosphere is also depicted. In addition, a list of innovative solutions which may help in bringing down the Pi application in agricultural systems also provided. AMFs; arbuscular mycorrhizal fungi, APase; acidic phoaphatase, GL; galactolipid; HATs; high-affinity, PAE; Pi acquisition efficiency, PPi; pyrophosphate, PHT; Phosphate transporters; PSMs; phosphate solubilizing microbes; PUE; Pi use efficiency, PHTs; Pi transporters, PL; phospholipids, SL; sulpholipid

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Table 1 Summary of the selected gene studies on the manipulation of purple acid phosphatases in plants
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Alteration related to Pi acquisition and transport

In plants, Pi uptake by roots (H2PO4− or H2PO42−) is maximum between pH 5–6. However, its uptake by roots is restricted by organic P assimilated in microbes and inorganic Al-P and Fe–P complexes in the soils. The acidic nature of soils, which account for ~ 30% of the total agricultural land worldwide, exacerbates this situation (Uexküll and Mutert, 1995). Further, due to the poor mobility of Pi (diffusion coefficient, 10−12 to 10−15 m2 s−1) in the soil, its active uptake by plants leads to a depleted Pi zone in the vicinity of roots (Furihata and Suzuki, 1992; Schachtman et al. 1998; Ullrich-Eberius et al. 1984). While Pi concentration in plant tissues ranges between 5–20 mM (Raghothama 1999), it remains mostly less than 10 μM in the soils (Bieleski, 1973). This massive difference in Pi concentration between plants and rhizosphere highlights the indispensable role of phosphate transporters (PHTs) in its acquisition. A suite of root-tip localized high-affinity Pi-transporters (HATs) is activated under acute Pi shortage in the soils (Poirier and Bucher, 2002). The PHT1 family of Pi-transporters is an excellent example of HATs. These proteins are highly conserved from fungi to plants. They are involved in the active transport of Pi from the soil to root hair cells (Nussaume 2011). Another class of protein, PHO1, containing the SPX-EXS domain, is critical to Pi transport from roots to shoots (Hamburger et al. 2002).

Intracellular Pi allocation and transfer between the cytoplasm and cellular compartments, including chloroplast, mitochondria, Golgi apparatuses, and vacuoles, contributes to Pi-homeostasis, especially under Pi deprivation. The non-metabolic vacuolar Pi is transported from the vacuole to the chloroplast (site of photosynthesis) and cytoplasm (site of glycolysis and sugar synthesis) under Pi deficiency (Poirier and Bucher, 2002). Different classes of transporters, PHT2 (chloroplast), PHT3 (mitochondria), PHT4 (Golgi apparatus), and PHT5 (vacuoles), are involved in such transfer and management of intracellular Pi pools (Sun et al. 2017). PHT5 class of Pi transporters is critical for the influx and efflux of Pi in and out of vacuoles (Liu et al. 2015, 2016). Recently, three vacuolar Pi transporters (VPTs), belonging to the SPX-MFS [SYG1/Pho81/XPR1 (SPX)-Major Facility Superfamily (MFS)] class, were identified in Arabidopsis. The biophysical studies on isolated vacuoles established PHT5;1 as the main vacuolar Pi influx transporter. Arabidopsis transgenic plants overexpressing this gene were found to sequester more Pi in their vacuoles. These plants also showed a higher vacuolar-to-cytosolic Pi ratio over their wild type controls, indicating importance of these genes to plant adaptation under nonuniform Pi availability in the soils. Similarly, PHT5 class members have been identified in rice. The functional studies revealed that OsSPX-MFS1 functions as a vacuolar Pi influx transporter, similar to its AtPHT5;1 homolog. Contrastingly, the other gene family member, SPX-MFS3, was found to function as an efflux VPT (Wang et al. 2015). For a more detailed outlook on PHTs, including gene expression, intracellular localization, and functions, two review articles recently published by Gu et al. (2016) and Wang et al. (2021a, b) are recommended for further reading.

Metabolic strategies for intracellular Pi homeostasis

Pi deficiency profoundly affects plants' carbon fixation, glycolysis, and respiration (Plaxton and Tran, 2011). Reducing the ATP demand to recycle and optimize internal Pi use is another metabolic strategy to mitigate its deficiency by plants (Cruz-Ramírez et al., 2006). Activation of inorganic pyrophosphate-dependent bypass enzymes is crucial for the metabolic adaptations of plants under depleted cellular Pi (Plaxton and Tran, 2011). Such changes facilitate the carbon flux for the enhanced synthesis of organic acids in the glycolytic pathway under chronic Pi limitation and help plant survival under depleted ATP levels (Plaxton and Tran, 2011). Up-regulation of alternative oxidases in mitochondria also contributes to such adaptation by maintaining the mitochondrial citric acid cycle and electron transport chain with impaired ATP production, especially under long-term starvation (Sieger et al. 2005; Plaxton and Podestá, 2006). During Pi starvation, enhanced sugar mobilization from shoot to roots occurs to support reprogramming of RSA (Hammond and White, 2008; Ciereszko et al. 2005). Further, root sugar levels seem vital for the secretion and activity of root-associated acid phosphatase as a mutation in a sucrose transporter gene (SUC2) lowered such activity in mutant Arabidopsis seedlings and impacted Pi uptake (Zakhleniuk et al. 2001). Emerging evidence suggests that exogenous sucrose supply under Pi starvation conditions enhances the activation level of several Pi starvation inducible (PSI) genes in plants, highlighting the importance of sugar signaling to PSRs (Karthikeyan et al. 2007; Akash et al. 2021; Srivastava et al. 2021; Khurana and Akash, 2021).

Remodeling of membrane lipids is another prominent alternate mechanism for Pi uptake under its acute deficiency. In such conditions, membrane phospholipids are converted into galactolipids. First, phospholipids, such as phosphatidylcholine, phosphatidylserine, phosphatidylethanolamine are converted into diacylglycerol (DAG), which is then converted into galactolipids such as monogalactosyldiacylglycerol (MGDG) or digalactosyldiacylglycerol (DGDG). MGDG and DGDG synthetases catalyze these reactions (Nakamura 2013; Okazaki et al. 2013; Pant and Burgos, 2015). A recent article published by Dissanayaka et al. (2021) has provided an in-depth overview of metabolic adaptations during PSRs in plants, including the mechanisms underlying phospholipid to galacto- and sulpholipid conversation under Pi starvation.

Strategies for improving Pi-use-efficiency (PUE)

Alternate Pi-sources and its recycling

Unearthing alternate Pi sources is critical to reducing over-reliance on the import of RPs. For example, phosphite (Phi), which has a higher solubility in water and is less prone to fixation in the soil, may be exploited as an alternate Pi-fertilizer (Heuer et al. 2017). Attempts have been made to develop bioengineered plants with the potential to utilize Phi as Pi-fertilizer (López-Arredondo and Herrera-Estrella, 2012). Expression of phosphite oxidoreductase (ptxD) enzyme coding gene in Arabidopsis helped transgenic plants efficiently convert Phi to Pi after its uptake by the roots. These bioengineered plants only required 50 to 70% of the original Pi input to achieve maximum productivity with Phi. Likewise, nuclear expression of ptxD in C. reinhardtii rendered transgenic lines the advantage of successfully metabolizing Phi as its Pi source(Loera-Quezada et al. 2016). Nonetheless, the natural inability of plants to metabolize Phi combined with high production cost and toxicity remains a bottleneck in its way to become a sustainable alternative to Pi-fertilizers. Further, due to its herbicidal properties, the use of Phi is banned in several European countries. Although the usage of Phi as an alternative Pi-fertilizer under the present scenario seems unrealistic, the development of Phi metabolizing plants which offers an alternative strategy to target both Pi nutrition with weed control cannot be neglected (Thao and Yamakawa, 2019; Heuer et al., 2017; Manna et al. 2016).

The amount of annually produced organic waste in big developing countries is enormous. Several available innovative technologies could be helpful for recycling and extracting Pi from urban, industrial, and agricultural waste. A few such technologies are already in place in Europe. For instance, sewage sludge ash is considered one of the best Pi sources across many European countries. Theoretically, it could meet 40–50% of annually applied Pi-fertilizer input in agriculture in central Europe (Egle et al. 2016; Zoboli et al. 2016). However, one of the biggest concerns about recovering Pi from municipal waste is its contamination with heavy metals and organic micropollutants. Therefore, modern techniques should be explored to recover Pi from sewage sludge with minimum contaminants. A cue in this context can be taken from a recently published article by Egle et al. (2016). The authors compared a total of 19 relevant Pi recovering technologies by considering their relationships with existing wastewater and sludge treatments. The outcome indicates that while clean and plant-available Pi is recoverable from municipal wastewater, the overall recovery remains poor. The present situation demands further technological innovations to improve the efficiency of the comprehensive Pi reclamation.

Identification and development of P-use-efficient crops

As per the definition by Hammond and White (2008), PUE is defined as the amount of total biomass or yield produced per unit of absorbed P. Plants are unable to assimilate majority of the applied Pi-fertilizers (Syers et al. 2008). One of the effective measures that have been suggested to significantly bring down the scale of Pi-fertilizers input in agricultural systems is the identification of crop germplasm with better internal PUE and Pi-acquisition. The high PUE genotypes would efficiently mobilize residual soil P. Although PUE involves a complex set of plant traits, two basic mechanisms are central to it. First, the root's ability to reclaim residual Pi from the soil (also known as Pi-acquisition efficiency, PAE; or external PUE). Generally, crops germplasm with higher P scavenging capacity is recommended for soils particularly rich in organic P and insoluble Pi-complexes. Second, the efficiency of internal remobilization of Pi for sustainable biomass production (also known as the internal PUE). In the second scenario, crop genotypes which can give better yield in under-fertilized soils are recommended (Lynch 2007). While identifying crops germplasm with better PAE can immediately bring down the amount of Pi-fertilizers used in agricultural systems, the development of enhanced internal PUE crops holds a long-term and more desirable sustainable solution (Rose and Wissuwa, 2012). It has been suggested that improving internal PUE (i.e. economic use of P in plants) for the better utilization of already available internal Pi pool for biomass production could prove a more resource-efficient approach in plants (Veneklaas et al. 2012). For example, high concentrations of P in cereal grains (largely present in the indigestible bound form as phytate) remains underutilized by human and animals. Therefore, developing cereal crop genotypes that accumulate less phytate in their grains but with similar yield potentials would lower P extraction from soils, requiring subsequently less Pi-input to restore soil P balance in the next crop cycle.

Although external PUE accessions are known for several crops such as maize, rice, legumes, Brassica, more efforts should be made to identify such germplasm for all crops (Ganie et al. 2015). For identification of high PUE crop accessions, root architectural traits for enhanced Pi foraging capacity, such as increased number of lateral roots/lateral root branching, denser and longer root hairs, more crown/proteoid/cluster/adventitious roots with shallower growth angles of growth have been suggested (Lynch 2007; Peret et al., 2014). For example, both longer and more dense root hairs are an attribute of Pi-efficient genotypes of common bean (Yan et al. 2004). More lateral roots by plants under Pi deficiency improve possibilities of P scavenging (Lynch 2007). However, such phenotypes may not always confer increased Pi uptake capacity in all crops. Further, monitoring these traits in the soils remains highly challenging. While increased branching capacity of plant roots may enhance their nutrients foraging capacity, this approach might only partially mitigate the P demand due to the heterogenous distribution of P in the topsoil. Therefore, engineering plants roots responding only to P-enriched patches in the context of a higher number of lateral roots or localized higher root hair density in low P soils may offer a better strategy (Richardson et al. 2011; Van et al. 2016).

To identify high PUE genotypes, the rhizosphere can be further analyzed for root exudates, mainly for the protons, organic acids, and hydrolytic enzymes. Pi-efficient genotypes in several plant species may release a higher volume of organic acids in the rhizosphere than the Pi-inefficient genotypes (Lyu et al. 2016). In a recent study, Wen et al. (2019) investigated root functional traits under Pi deficiency in 16 crop species and reported that substantial interspecific variations exist for these traits among the species. For examples, species with thinner roots relied more on intense root branching for Pi scavenging whereas species exhibiting thicker roots depended more on the secretion of root exudates for the mobilization of bound P in the rhizosphere (Wen et al. 2019). Similarly, Lyu et al. (2016) rep orted that legumes such as white lupin and chickpea, lacking the fibrous roots (present in cereal species) relies more on exudation of organic acids to mobilize Pi in the rhizosphere than wheat and maize. A root exudation index has been proposed to be useful biomarker for the identification of genotpes with enhanced PAE (Dissanayaka et al. 2021). However, during such screening, care must be taken as this trait is insufficiently consistent and may vary among plant species. For instance, Pearse et al. (2007) reported that despite the exudation of citrate, pea could not mobilize Pi from Al-P and Fe–P complexes. It has also been observed that organic acids become unstable in both acid and calcareous soils and quickly lost after degradation (Wang et al. 2010). Several attempts have already been made to improve PUE in multiple crops. In this context, Zhang et al. (2014a, b) have provided information on candidate genes that have been been explored to improve PUE in different crops. Although genotypes with the enhanced secretion of organic acid in the rhizosphere seems an exciting choice, however, it has been reported that in some species the metabolic investment of the plants in producing these exudates is quite substantial (Lynch and Whipps, 1990; Nguyen 2003; Rees et al. 2005). In some Proteaceae members and white lupin, the volume of secreted products may amount for ~ 25% of whole plant dry weight (Gardner et al. 1983; Dinkelaker et al. 1989). In white lupin, up to 25% of total photosynthetes are diverted as sucrose to cluster roots by Pi-depleted plants to support the enhanced root exudation in the rhizosphere (Canarini et al. 2019). Especially under Pi stress, rice root exudates attributed to 2–3% of total plant biomass (Kirk et al. 1999). For minimizing the carbon costs, the alternative respiratory pathway that is non-phosphorylating in nature (cyanide resistant pathway and rotenone insensitive pathway) should be focused. This pathway allows respiration to proceed without depleting phosphate or adenylate pools and is induced under Pi-deprived conditions (Rychter et al. 1992; Theodorou and Plaxton, 1993). Similarly, shifting the biomass allocation towards metabolically efficient root classes, such as adventitious roots, can also enable us to efficiently utilize the soil Pi reserve (Miller et al. 2003).

Alternatively, improving more efficient internal P usage under its unavailability offer a better solution. Genotypes with effective P mobilization within plants, such as its mobilization from mature/senescing organs to newly emerging/actively growing organs or its recycling between vacuoles and cytoplasm for most crops, must be identified. Akhtar et al., 2008 demonstrated that efficient Pi internal mobilization contributed to the high PUE observed in some Brassica cultivars. Early growth and development of germinating seedlings are supported by seed stored P (White and Veneklaas, 2012). The high amount of seed/grain P in cereal crops remains under metabolized by humans and monogastric herbivores (Veneklaas et al. 2012). Therefore, developing crops with significantly lower seed phytate levels is often advised. However, low phytate levels may lead to compromised seed vigor, and targeted fertilization may overcome such a situation. For example, seed coating with Pi-fertilizers, especially the nano-formulations (such as nano-DAP; Singh et al. 2021) could provide a viable solution to compensate low seed phytate levels. Nonetheless, more investigations are needed to create such combinations of modified crops and nano-P formulations to assess their performance in agriculture.

Another area to improve internal PUE is by using specific phosphatases involved in internal Pi re-allocation. Acidic phosphatases (APases) are know to libertate Pi from its monoesters in a mildly acidic pH range (Tran et al. 2010; Srivastava and Akash, 2020). PAPs constitute the largest family of APases. Several PAPs are known to actvate under Pi limitation conditions in plants. Activation of PAPs in shoot marks their importance in mobilization of Pi form intracellular monoesters and anhydrides during Pi deprivation or leaf senescence (Tran et al. 2010; Plaxton and Tran, 2011). Similarly, activation of root-specific PAPs help mineralize Pi from its extracellular organic compounds and insouluble inorganic complexes in the rhizosphere. Although little is known about phosphatases involved in internal re-allocation of Pi, Tang et al. (2013) have reported activation of such a gene, LaSAP1, in the roots of Pi-starved white lupin. An Arabidopsis thaliana PAP, AtPAP26, has been found to be critical for vacuolar Pi recycling during Pi deprivation and leaf senescence (Robinson et al. 2012; Dissanayaka et al. 2021). Similarly, transcript abundance analysis of AtPAP17 gene using Klepikova Atlas, available at TAIR revealed its highly specific high expression in the senescent leaf (https://www.arabidopsis.org/servlets/TairObject?id=38109&type=locus). Such a gene could be an ideal candidate for investigating its role in determining internal PUE. Alternatively, enhancing PUE by tweaking plant metabolism to lower P demand, as described in the earlier section, can be explored. In this context, metabolic adjustments done by the members of Proteaceae under Pi deficit conditions are fascinating. One of the critical adjustments undertaken by these members includes an investment of lower Pi resources in rRNA synthesis, especially plastid rRNA. This adjustment does not favor the production of those enzymes which requires P-containing metabolites during carbohydrate metabolism. It also leads to delinking of growth from the synthesis of photosynthetic machinery during early leaf development. Altogether, these adjustments have been found to contribute to a high photosynthetic PUE in the Proteaceae species in comparison to Arabidopsis and crops (Sulpice et al. 2014). Further, the role of sugar signaling in controlling the scale of transcriptional activation of selected PSI genes is exciting and demands further research for a better understanding on the role of sugars in controlling PUE.

Microorganisms for facilitating Pi acquisition in plants

Soil-based microorganisms are important for mobilizing tightly bound soil P to promote its availablity in rhizosphere (Richardson et al. 2011). Two reactions determine Pi fixation and uptake in the soils. The first process involves fixation of Pi onto soil particles, whereas the second involves the solubilization of bound Pi from the available inorganic complexes and organic P present in the soils (Havlin et al. 2005). Over decades, the frequent use of chemical fertilizers has impacted soil health (Gyaneshwar et al. 2002). Long-term P fertilization adversely affects soil fungal and bacterial diversity in croplands (Beauregard et al. 2010; Chen and Liu 2019; Chen et al. 2019). Excessive fertilization also leads to problems like inhibition of substrate-induced respiration by acitidione (activity observed in bacteria) and streptomycin sulfate (activity observed in fungus) (Bolan et al. 1996). Similarly, triple superphosphate application led to reduced microbial respiration and metabolic quotient (Thirukkumaran and Parkinson, 2002). Co nsidering the side-effects of excessive Pi-fertilization, more environmentally benign approaches such as use of Pi-solubilizing microbes (PSMs) as microbial inoculants are routinely carried out to improve crop production.

A vast number of microbial species have been identified with excellent Pi-solubilizing capacity. Such diversity includes bacteria, fungi, actinomycetes, and some algal species. Among bacteria, Pseudomonas and Bacillus species are the most well-known Pi-solubilizers. Rhodococcus, Arthrobacter, Serratia, Chryseobacterium, Gordonia, Phyllobacterium, Delftia, Azotobacter, Vibrio proteolyticus, Xanthobacter agilis, Xanthomonas, Enterobacter, Pantoea, and Klebsiella are some of the other significant Pi-solubilizing bacteria (Cheng et al., 2011; Kumar et al. 2011; de Freitas et al. 1997; Vazquez et al. 2000). Another excellent example of a Pi-solubilizing bacterium is the symbiotic nitrogenous rhizobia Rhizobium leguminosarum bv. Trifoli. Besides nitrogen fixation, this bacteria has been reported to improve plant nutrition by mobilizing Pi from its inorganic and organic forms (Yanni et al. 2001). For a comprehensive account of the role of PSMs and strategies involved in facilitating Pi uptake, a recent review article by Rawat et al. (2020) is suggested for further reading.

Pi-solubilizing fungi consist of about 0.1 to 0.5% of the total fungal populations in the soils (Kucey 1983). Fungi are more suitable because these do not lose their Pi-solubilizing capabilities under laboratory conditions, which often limits the use of bacteria (Kucey 1983; Sperber 1958). Fungi traveling more distance (even beyond Pi depletion zones) in the soils via their hyphae greatly increases the possibility of P scavenging. AMFs directly deliver scavenged Pi to the root cortical cells (Bolan et al. 1991). In return, fungus obtains carbohydrates and lipids from the plant (Sawers et al. 2017). Almost 80% of plant species are known to have mycorrhizal associations (Schachtman et al. 1998). Hence, the solubilization of P present in the soil can be achieved more efficiently by fungi than bacteria (Kucey 1983). Since AMFs are naturally present in most soils, it is often difficult to notice their beneficiary role in Pi uptake in field conditions. Nevertheless, laboratory-scale pot experiments involving root colonization by AMF isolates under sterile soil conditions have revealed their positive role in Pi uptake by plants (Tawaraya, 2003; Deguchi et al. 2012). Among the filamentous fungi, Aspergillus and Penicillium species are the most significant Pi-solubilizers in the soils (Fenice et al. 2000; Khan et al. 2010; Reyes et al. 2002). A few Rhizoctonia solani and Trichoderma strains have also been reported as efficient Pi-solubilizers (Altomare et al. 1999; Jacobs and Boswell, 2002). Re cently, Srivastava et al. (2021) reported the positive role of Glomus species inoculation on barley seedlings' growth under the P-optimum nutritional regime. The AMFs-inoculated barley seedlings accumulated higher biomass with less Pi accumulation. Authors observed significantly enhanced PUE in the AMFs-colonized seedlings over their non AMF controls. While low Pi conditions support plant-AMFs interaction, high soil P conditions are often unfavourable for mycorrhization, although to varying degree in different species (Baylis 1967; Mosse et al. 1973; Johnson 1993; Van Geel et al. 2016). It is important to mention that the degree of success between plant-fungus association is influenced by host genetic factors as well; which tend to vary greatly with the change in the host species. A better understanding of the mechanisms underlying mineral uptake in croplands, especially host factors influencing plant mycorrhiza-mediated mineral nutrition, could be used to develop strategy for a resource-efficient sustainable agricultural system. Two recent review articles published by Sawers et al. (2017) and Kobae (2019) are recommended for further reading to understand the dynamics of the plant-fungus symbiotic associations.

Altogether, the collected evidence demonstrates that the native microbes in the rhizosphere help improve nutrient uptake. However, their commercial application as bio-inoculants has produced mixed results. One of the reasons for this observation could be that an alien microbe species, used as a bio-inoculant, can compete with native microbes of the rhizosphere and limit their overall nutrient-use efficiency. Therefore, knowing native microbe populations associated with different crops is a prerequisite before using any microbe as a bio-inoculant. Recent metagenomics studies providing insights into the structure and biodiversity of rhizosphere microbiomes for different crops in different soils are encouraging. Such information is useful to understand co-evolved diversity and host-microorganisms dynamics. For example, Chalasani et al. 2021 recently showed that non-symbiotic Rhizobium spp predominantly colonizes pigeon pea roots, rather than symbiotic Bradyrhizobium spp in Indian soils. Additionally, the data provided insights into the factors controlling pigeon pea bacterial community structure. Plant fraction, followed by developmental stage, soil type, and although the least important yet still a significant factor, plant genotypes influenced the bacterial community. Similarly, a genome-wide association study targeting to understand population-level microbiome analysis of the rhizospheres of 200 sorghum genotypes revealed a putative plant loci that control the heritability of the rhizosphere microbiome (Deng et al. 2021). Such data would be useful in devising effective ways to utilize species-specific bacterial/fungal partners to improve overall fertilizers' nutrient-use efficiency.

Nanofertilizers

The currently used chemical fertilizers have a major problem with their agronomic efficiency (Kah et al. 2018). Currently used mineral fertilizers are inefficient and needed in substantial quantity to support agricultural systems. Moreover, the granular forms need a massive amount of water for their dispersal. Advanced technology-based solutions such as nanotechnology are being explored to improve the delivery of the plants' macro-and micro-nutrients (such as P, N, and Zn). For instance, the application of urea-hydroxyapatite nanohybrids (for the slow release of nitrogen) in the rice fields significantly enhanced the agronomic use efficiency of urea. The field trial data clearly showed that the nanohybrids were translated directly to enhanced plant availability and growth while reducing the nitrogen content used by up to 50% (Kottegoda et al. 2017). Similarly, we also noticed the promotion of vegetative growth of monocot and dicot species after applying a reduced amount of cryo-milled diammonium phosphate nanoparticles (nDAP) over granular DAP (Singh et al. 2021). In this novel approach, the cryo-milling method was used to produce ~ 5000 times smaller particles of nDAP over the granular DAP (cDAP). A comparative study using different concentrations of nDAP and cDAP to investigate their effects on plant growth showed cDAP grown tomato and wheat seedlings being outperformed in biomass production by their equimolar nDAP grown counterparts. The nDAP grown seedlings consistently accumulated more Pi than their cDAP grown controls in all concentrations, indicating the beneficial role of reduced-sized Pi-fertilizers in plant growth promotion (Singh et al. 2021).

Precision farming

Precision agriculture is the method of implicating innovative and efficient technological advancements into agriculture for its betterment. Among the different environmental elements, the soil is the most exposed component in terms of excessive fertilization. Incorrect dosage or over-fertilization can increase soil salinity and acidity and also increase the risk of heavy metal contamination. Precision agriculture shows the way of appropriate fertilizer application by firmly moderating fertilizer doses based on the plant species. It also enables the application of fertilizers based on weather conditions and soil conditions (Adamchuk et al. 2004; Mikula et al. 2020). Whereas this approach has been discussed for micronutrient delivery, with emerging macronutrient nano-formulations, the concept for a more controlled delivery of these fertilizers holds a promising future. In this context, Indian Farmers Fertiliser Cooperative Limited (IFFCO), an Indian fertilizer company, has launched the world's first environment-friendly nano Urea (liquid) fertilizer (https://iffco.in/assets/images/IFFCO-Nano_PressNote-converted.pdf). Approximately, 10,000 times smaller nanoscale nitrogen particles than a Urea pril constitute the liquid fertilizer solution. As per the available information, the uptake efficiency of nano Urea is significantly increased over its prill form. Besides higher nutrient use efficiency, nano Urea is expected to reduce soil, water, and air pollution (https://iffco.in/index.php/ourproducts/index/nano-urea). The implication of Slow Released Fertilizers (SRFs) and Controlled Release Fertilizers (CRFs) can aid the nutritional needs of the plants while preventing excessive applications. Metaphosphates, glassphosphates have provided significant beneficiary results in terms of SRFs (Arslanoglu, 2019). Al together, the application of nano fertilizers would prove to be a big step towards the ultimatum of sustainable agriculture (Mikula et al. 2020).

Comprehensive national policy on P import, use and recycle

Sustainable P-reserves for the future depends on innovative ideas and actions. Creative solutions can ensure the continued availability of Pi-reserves to agriculture. The uninterrupted supply and sustainable Pi-use will require several factors to consider, including.

  1. i.

    Global, local, and integrated P management are necessary for P-poor countries to ensure the benefits and cost of production getting distributed equitably.

  2. ii.

    Crop germplasm with improved PAE and internal PUE needs to be identified to maximize the agricultural produce.

  3. iii.

    Innovative farming technologies and farmer education regarding sustainable agriculture can also help to maximize sustainable Pi-use.

  4. iv.

    Maximization of knowledge transfer and communication between stakeholders, commercial industries, and sectors like mining and fertilizer industries is essential. A collective effort from every sector can only guarantee the sustainability of Pi.

Sustainable Pi-use in Europe: a case study

  1. i.

    A city-level study conducted in Gothenberg, Sweden, suggested a possible management strategy to separate 70% of the food waste from households and business sectors (Kalmykova and Strömvall, 2012). Th e city was estimated to produce 88 tons of P annually, which could return to agriculture after reclamation. It was further noticed that the implementation of the urine diversion also has similar potential. Segregation of blackwater and food waste could provide the best results regarding the complete recycling of P-based nutrients. The authors estimated the potential for the annual recovery of 245 tons of Pi from different city waste products for agriculture.

  2. ii.

    Recently, De Buck et al. (2012) suggested another action plan on a country basis by studying the Netherlands' agricultural system. The authors considered a range of scenarios that could return the surplus Pi to the farming fields. The improved farming solutions include removing excess Pi from the harvested products, balanced fertilization techniques, and feeding concentrates for livestock containing 10% less Pi.

  3. iii.

    The P-Rex project in Europe implemented new technologies for recycling and the sustainable use of Pi. This project demonstrated technical solutions regarding the recovery and recycling of Pi in full scale. The P-Rex project continued till 2015 and has hugely benefitted the Pi-reserves throughout the continent (Schoumans et al. 2015).

  4. iv.

    Numerous technologies such as Air prex, ANPHOS, Aarhus Water, Budenheim, LysoGest, Nuresys, PEARL, Phospac, P-ROC have been widely used in different European countries to obtain Pi-from the wastewater (Schoumans et al. 2015). Products like Struvite, CaP, P mineral, DCP, P4 have been used as agents to separate P and P-based compounds from wastewater in these processes.

Conclusions and future perspectives

The increasing demand, high price, soil health, and environmental consequences of intensive Pi fertilization along with finite nature of natural rock phosphate reserves demand more efficient use of this resource in agricultural systems. Unlike the other non-renewable resources such as fossil fuels, where alternate strategies are already available; Pi-fertilizers have no alternative or replacement (Herrera Estrella et al. 2016). P shortage is being speculated to challenge food security in the future. Such a crisis could be more severe in countries lacking large indigenous P-reserves (Subba Rao et al. 2015). The present situation demands urgent development of a proper, holistic policy on P-management in agrosystems. The action plan should integrate all possible strategies, including reclaiming and recycling Pi from organic matter and urban and industrial waste. Simultaneously, low Pi-tolerant or Pi-use-efficient crops germplasm should be identified or developed. The development of agronomically superior fertilizers such as nano Urea and nano-DAP is critical to bringing down fertilizers' application in agrosystems. Additionally, the targeted delivery mechanisms such as mixing Pi-fertilizers with seeds before sowing are highly desirable and should be aggressively tested. Altogether, innovative sustainable techniques for reclaiming P from industrial, domestic, and agricultural waste, agronomically superior Pi-fertilizers alongwith high PAE/PUE crops germplasm hold the key for prolonging P-sustainibility in the future.