Introductory Chapter: Phosphorus in Soils and Plants

1. Introduction

Plants (crops), soils, and humans are intricately interrelated. As heterotrophs, humans (and animals) largely depend on plants and/or on the plant-associated food resources. Seventeen (17) nutrient elements are varyingly required by plants in optimum level for the maintenance of their growth, metabolism, and productivity, as well as for their sustenance under adverse conditions. These elements are also called nutrients and include carbon (C), hydrogen (H), oxygen (O), nitrogen (N), phosphorus (P), potassium (K), sulfur (S), calcium (Ca), magnesium (Mg), boron (B), chlorine (Cl), copper (Cu), iron (Fe), manganese (Mn), molybdenum (Mo), nickel (Ni), and zinc (Zn). Interestingly, N, P, K, S, Ca, Mg, B, Cl, Cu, Fe, Mn, Mo, Ni, and Zn are derived from the soil (or parent rock materials) and can also be supplied by fertilizers. On the other hand, the list of non-minerals includes C, H, and O since these elements are obtained from water, air, or both. In addition to nourishing the plants, soils also provide anchorage, air (O₂), water, temperature modification, and the stabilization. As an essential plant macronutrient, P has been a key regulatory element for plant growth and metabolism. Unfortunately, P-bioavailability has been a worldwide constraint for plant growth and productivity. There must be a fine P-homeostasis in the soil-plant system in order to maintain the status of the soil-P and its efficient uptake and metabolism in plants, for optimum plant growth and productivity and eventually for attaining agricultural and environmental sustainability and the global food security.

2. Phosphorus in soils

Phosphorus (P; atomic number 15; nonmetal; placed in the 3rd row of the periodic of the elements; discovered by German chemist Hennig Brand in 1669) is a chemical element that occurs as white P and red P, its most common allotropic forms. It is never found as a free element on Earth and generally occurs as phosphates (PO₄³⁻). P has 22 known isotopes which range from ²⁶P to ⁴⁷P [1]. Notably, ³¹P is the only stable isotope of P and is therefore present at 100% abundance. Apatite (comprising minerals pentacalcium triorthophosphate fluoride) partly constitutes inorganic phosphate rock, the chief global commercial source of P, and a nonrenewable resource for the phosphate fertilizers.

Ranked 11th in the list of most abundant elements in the environment, P is neither easily accessible nor evenly distributed in most soils. In addition, the availability of the soil-P to plants/crops is limited. The concentration of P in the soil solution can be very high (10⁻⁴ M), very low (10⁻⁶ M), or as low as 10⁻⁸ M in some very poor tropical soils. Though P is not available in gaseous form, it is available in both inorganic and organic forms in the soil. In general, soil-P is available in both organic form (about 30–65%) and inorganic form (about 35–70%). Notably, plant-available (soil solution) P, sorbed P, and mineral P are the major pools of inorganic P-form. Contingent to the pH, H₂PO₄⁻, HPO₄²⁻, and PO₄³⁻ are the major P-forms in the soil solution. P exhibits very low solubility and poor mobility in soil solution, as well as its capacity to form insoluble salts with different mineral elements. Soils with low amounts of organic matter and low water holding capacity are usually nutrient-deficient acidic soils widely reported to exhibit the least mobility of P as well as the least availability to plants (compared to N and K). P is also incorporated into organic compounds, where about 20–80% of soil-P is present in organic matter mainly as phytic acid (inositol hexakisphosphate), which can bind to various anions resulting in the formation of phytate. Most soil-organic P pools (mostly composed of plant and microorganism residues and livestock manures) cannot be absorbed directly by most plants [2]. Hence, P is among the less accessible elements for most plants [3]. H₂PO₄⁻, denoted by inorganic phosphate (orthophosphate; Pi), dominates in the pH range of 3–7 and is the predominant form absorbed by plants. On the other hand, ester derivatives represent the organic P present in organic molecules. Phosphates are not reduced; however, the oxidized form of P is incorporated in the biomolecules [4]. There are several factors (physical, chemical, and biotic) known to regulate P-availability in soils and to the plant roots for its uptake. Major P-availability-modulating physical factors include soil texture and moisture; whereas chemical factors can be the soil solution pH, organic matter, redox potential, P-concentration in the soil solution, P-buffer capacity of the soil, and the concentration of Fe, Al, and Ca. On the other hand, major biotic factors influencing the plant/crop root activity and the P-release in the rhizosphere include the diversity of microorganisms [5, 6, 7, 8].

3. Phosphorus in plants

In terms of its importance in most organisms, P has been considered an essential, irreplaceable element in all living cells. P stands second to N in terms of its essentiality as a macronutrient in plants/crops. P has been widely considered as a key regulatory element for plant growth and metabolism. Apart from providing an anchor for the plant in the soil, roots take up water and nutrients from the soil solution. In fact, the interception of nutrients available in the soil solution occurs in the rhizosphere. Eventually, the movement of nutrients toward the root involves mass flow and diffusion, where the former process contributes only 2–3% of the total amount of P (transported), usually required by many crops to produce acceptable yields. Interestingly, Pi, the only form of P that can be assimilated by plant, exhibits uneven distribution, relative immobile (as its diffusion coefficient is very low: 10^–12 to 10^–15 m² s⁻¹), and high fixation. Hence, the concentration of Pi is very low (<2.0 μM) in soil solution, and even in fertile soil (10 μM). In plants, P represents 0.1–0.5% of the dry weight. Therefore, Pi-availability has been a worldwide constraint for crop growth and productivity [3].

The knowledge of the plant Pi-acquisition and distribution mechanism may help in enhancing the plant/crop P-use efficiency. The list of the major strategies adopted by most plants/crops under P-deficiency includes: (i) increase in root surface area by formation of finer roots, aerenchyma, and root hairs, and eventual improved soil exploration; (ii) secretion of organic acids to release Pi through complexation reaction of organic acids with Al³⁺, Fe³⁺, and Ca²⁺; (iii) the complexation reaction of organic acids with phosphatases to release Pi from the organic sources and thus to enhance the availability of Pi in soils; (iv) arbuscular mycorrhizal fungi (AMF) colonization; and (v) employing Pi transporters to facilitate Pi-uptake [3, 9, 10]. Arbuscular mycorrhizal fungi (AMF; phylum Glomeromycota) contribute to plant P-nutrition. Notably, AMF-colonization process is modulated by Pi-status and PHT1 transporter. Interestingly, this AMF-colonization is usually not well developed in soils with adequate, plant-available P. Both terrestrial plant species (90%) and in particular vascular plants, including main crops (>80%), exhibit AMF-colonization. Molecular genetic studies have unveiled various Pi-transporters, which facilitate the plant uptake and translocation of available Pi. Five phylogenetically distinct classes of families of plant Pi-transporters are known: PHT1, PHT2, PHT3, PHT4, and PHT5. PHT1s are, in general, plasma membrane-located and mainly function in Pi acquisition from soil. PHT2, PHT3, PHT4, and PHT5 family members are known to contribute in Pi distribution within the plant such as translocation against chloroplasts, mitochondria, Golgi, and vacuole. PHT1 transporters, the best studied plant Pi transporters, belong to multigene family and are involved in transport of Pi from apoplast/soil solution to the root cell through the plasma membrane [11]. Under P-deficiency/starvation, P-starvation response (PSR) pathway is activated, which involves PHOSPHATE TRANSPORTER TRAFFIC FACILITATOR1 (PHF1) and PHT1, and several transcription factors including PHOSPHATE STARVATION RESPONSE 1 (PHR1) and PHR1-LIKE 1 (PHL1), WRKY74, WRKY75, MYB2, MYB4, and ARF16 have been associated with the PSR pathway and implicated in P uptake [2, 12, 13]. Organic esters (such as phosphomonoesters and diesters) are the organic forms of P in plants. Phytase-mediated release of phosphates from phytates is possible during seed germination. Organic forms of P (namely, phosphomonoesters and diesters) are broken in plants by enzymes, namely, phosphatases and diesterases, in order to make P available to plants [4]. Plant responses to the low P (or P-starvation) also involve several hormones and signaling molecules (including cytokinins, CKs; abscisic acid, ABA; gibberellin, GA; and strigolactones, SLs) [14].

Interestingly, essential biomolecules such as DNA, RNA, ATP, NADPH, and membrane phospholipids involve P. In fact, nucleic acids, phosphorylated proteins, various phosphorylated metabolites, and phospholipids present the major pool of organic-P. Hence, plant tissues exhibit relatively high (about 5–20 mM) phosphate concentration. Phosphatases, nucleases, and phosphoesterases have been reported to contribute in the release of Pi from the organic forms during senescence in plants. Additionally, photosynthesis, respiration, and activation of proteins via phosphorylation, the life-sustaining processes in plants, strictly involve P. P is irreplaceable in many P-containing biomolecules. ATP and NADPH are the major high energetic molecules and are prerequisites to ensure photosynthesis functioning during the Calvin cycle [15]. Literature is full on the role of P in plant cell metabolism. The regulatory mechanisms during the developmental processes as well as response to stress conditions in plants involve phosphorylation of proteins. Moreover, intermediates in Calvin–Benson cycle are phosphorylated with Pi. Pi is released in the cytosol and is cycled back to plastids. The availability of Pi regulates photosynthesis, which is inhibited with limited Pi-supply. A plethora of literature supports the significant roles of P in imparting plant/crop tolerance to various abiotic stresses including drought [16, 17, 18], heavy metals [19, 20, 21, 22], soil salinity [23, 24, 25, 26], temperature [27, 28, 29, 30], and water logging [31, 32].

4. Environmental concerns

The productivity of many agroecosystems is largely modulated by plant P-nutrition. Unfortunately, mainly as a result of phosphate extraction, fertilizers application, wastes generation, and P-losses from cropland, humans have perturbed the global P-cycle, which has tripled the global P-mobilization in land–water continuum and also increased P-accumulation in most soils [33]. Owing to the importance of P to life, and the considering the soil to water-sourced P as the major contributor for eutrophication in surface water bodies (and also in natural terrestrial habitats), the maintenance of the P-status of most world soils and its efficient use in agriculture have been focused in recent years. In particular, to attend the prevailing very low availability of Pi for plants/crops, intensive fertilization of crop plants with P-fertilizers (mainly as N-P-K fertilizers globally) is being adopted. Unfortunately, only 10–20% of applied Pi can be absorbed by plants, and rest can remain in the soils as legacy P. Thus, mainly intensive fertilization of crop plants with P-fertilizers has both impeded phosphate rock (non-renewable resource); and has also increased the fertility status of natural waters (eutrophication) due to legacy P (past P surpluses) in soils, sediments, and wastes. Elevated P levels in eutrophic water bodies cause increased growth of algae and large aquatic plants, leading to decreased levels of dissolved O₂, and/or algal toxin (produced by algae blooms) and eventual severe impacts on the health of aquatic biota, as well as that of humans and animals. The feeding of the crops with P but not the soils has been suggested in order to properly manage P in the food chain [34]. Thus, unscientific use of fertilizers has eaten away most soil nutrients, disturbed the soil-P balance, inhibited healthy plant growth, and provoked eutrophication and thus has become a major concern in sustainable agriculture production systems worldwide.

5. Conclusion and prospects

Among several nutrient elements that are varyingly required by plants, P is the major macronutrient involved in the maintenance of growth, metabolism, and productivity of plants, as well as for their sustenance under adverse conditions. Unfortunately, P is among the less accessible elements for plants mainly as a result of its very low solubility and poor mobility in soil solution, as well as its incorporation into organic compound. The availability of soil-P is modulated by several physical factors (soil texture and moisture), chemical factors (soil solution pH, organic matter, redox potential, and the concentration of Fe, Al, and Ca), and biotic factors (diversity of microorganisms in rhizosphere). Most plants/crops under P-deficiency adopt a range of strategies to facilitate plant/crop P-use efficiency. Pi-uptake and root-to-shoot transport are mediated by both low- and high-affinity Pi-transporters, whereas Pi-redistribution at tissue, cellular, and subcellular levels is facilitated by a dedicated sets of transporters. In addition to performing key functions in plants (such as energy transfer, photosynthesis, transformation of sugars and starches, and nutrient movement within the plant), an adequate P-supply help plants to sustain, develop, and produce under varied abiotic stress factors.

The knowledge of P-recycling and -mobilization may help in improving plant/crop P-use efficiency and thereby minimizing the P-fertilizer input to the environment. In particular, appropriate fertilizer encompassing both the change in the amount and suitability of P-fertilizer, as well as deciding the rate, time, and place of P-fertilizer, may help in achieving sustainable crop production. Exhaustive molecular genetic studies on P-solubilizing microorganisms, understanding Pi-transporters in tonoplast and Pi-uptake by the cells not symplastically connected to guard cells or the developing embryo, and identifying proteins mediating Pi-transport across tonoplast will be promising in the research area aimed at unveiling insights into P in soils and plants.