Phosphorus (P) deficiency represents a major mineral nutrient deficiency in agricultural soils affecting crop production. Plants absorb P mainly in the form of orthophosphate ions (i.e., H2PO4– and H2PO4-2); however, availability of orthophosphate ions to plant roots is often extremely low in soils.
Phosphorus Deficiency in Soils
Indeed, P is rich in soils; but its phytoavailability to plants is adversely affected by various chemical and biological processes. When applied to soil, P fertilizers are very rapidly immobilized and transformed into insoluble P forms such as calcium-phosphates in high pH soils and aluminium- or iron-phosphates in low pH soils as shown below (Hinsinger, 2001 Plant and Soil. 237:173-195; Richardson et al., 2009, Crop Pasture Sci. 60: 124–143; Penn and Camberato, 201, Agriculture, 9, 120). Published reports indicate that only less than 20 % of the applied fertilizer P is absorbed by the plants while the remaining is immobilized and unavailable for root uptake due to rapid conversion of fertilizer P to insoluble forms.
Microbial immobilization of P is a further soil phenomena which makes fertilizer P unavailable for root uptake, at least, temporarily. Soil microorganisms compete with plant roots for available P and immobilize it in their biomass (Richardson and Simpson, 2011, Plant Physiol. 156: 989-996). It is, therefore, not surprising why the phytoavailable (soluble) concentration of inorganic phosphorus (Pi) in soil solution is often too low (around 2 µM) which is roughly 10 000 times lower than the Pi concentrations existing in root cells (Plaxton and Tran, 2011, Plant Physiol. 156: 1006–1015). It is interesting to note that root cells maintain very high Pi concentrations (at millimolar levels) while soil solution contain Pi at low micromolar levels. This suggests that plants develop highly efficient root strategies for P acquisition from soils (Hinsinger, 2001 Plant and Soil. 237:173-195; Lynch, 2011, Plant Physiol. 156: 1041–1049). This topic will be discussed in a separate article.
Figure 1 sows that over 50 % of the agricultural soils are adversely affected from low amounts of phytoavailable P and exhibits a high P retention/immobilization potential (Kochian 2012, Nature, 488:466-467). Majority of P existing in soil is tightly held or fixed by the soil particles and not useful for the root uptake. Depletion of phytoavailable P through intensive cropping and soil erosion is a further critical issue leading to soil P deficiency, in particular in low input farming systems (Tan et al., 2005, J. Sustain. Agric. 26:123-146; Alewell et al., 2020, Nature Comm. 11:4546). According to Alewell et al. (2020), P losses from soils through erosion may exceed 20 kg ha-1 yr-1).
Figure 1. Global distribution of soils differing in degree of phosphorus retention (immobilization) potential (i.e. phosphorus is tightly bound to soil particles or fixed in soil organic material) (Kochian 2012, Nature, 488:466-467).
In soils having very high P fixation capacity and low amounts of phytoavailable P, plant growth is often depressed leading to significant impairments in growth and yield capacity of crop plants as shown below in Figure 2 for rice grown under field conditions in Tanzania and USA and maize in USA. The experimental plants respond very positively to application of P fertilizers with better biomass production and grain yield formation. The rice trials conducted by Dr J. Harrell in Louisiana showed increases in grain yield up to 50 %.
Figure 2: Growth of rice plants in Louisiana in USA (top) and in Tanzania (below left) and maize plants in USA (below right) with low and adequate P fertilization (see https://www.ricefarming.com for rice trials by Dr J. Harrell in Louisiana; africarice.blogspot.com for rice experiment in Tanzania by Dr De Bauw and Plantsagronomy.k-state.edu for maize experiments)
Functions of Phosphorus in Plants
Phosphorus: a basic element in vital cell compounds
Phosphorus has diverse physiological and biochemical function in plants. There are several basic compounds in cellular systems which require P for their structure and biological functions including DNA, RNA, ATP, NADPH and phospholipids.
Phosphorus is required in energy transfer and storage through ATP (adenosine triphosphate) in biological systems and contributes to synthesis and stability of DNA and RNA. Similarly, as a basic component of membrane phospholipids, an adequate P nutrition is also essential for the structural and functional integrity of cell membranes (Hawkesford et al., 2012, In: Mineral nutrition of higher plants. Elsevier). Phospholipids are the major component of cell membranes, required for structural stability and function and affect the membrane transport systems. Under P deficiency, structural impairments in cell membranes can be expected with adverse effects on nutrient transport across the root cell membranes NADPH serves as a major provider of reducing equivalents in cellular systems and plays diverse critical roles including regeneration antioxidant defence systems . Below a few critical physiological functions of P in plants are introduced and discussed.
Phosphorus in photosynthetic carbon metabolism
There are several reports dealing with the role of P in photosynthetic carbon (C) metabolism and production of photoassimilates. Majority of the reports indicate very critical functions of P in photosynthesis process. As a structural component of various sugar phosphates such as ribulose-1,5-bisphosphate (RuBP) and fructose 6-phosphate, P greatly affects photosynthetic CO2 fixation. Under low P nutrition, impairment in RuBP regeneration is a well-documented result which diminishes Rubisco activity and consequently CO2 fixation (Hammond and White, 2008, J Exp Bot 59: 93–109; Warren 2011, Tree Physiology 31, 727–739) The regeneration of RuBP in chloroplasts is an ATP-dependent process, and, as discussed below, the pool of ATP is very low in P deficient plants.
Orthophosphate ions (i.e., inorganic phosphates; such as H2PO4–) are important players in photosynthetic carbon metabolism and used as substrate for ATP synthesis through the photophosphorylation process. As expected, P deficiency is often associated with low concentration of orthophosphate ions (Pi) in chloroplasts which results in impairment in ATP production through the reduced ATP synthase activity (Figure 3; Carstensen et al.,2018, Plant Physiol 177:271–284).The adverse impact of low P on ATP formation is highly Pi specific and is rapidly restored after application of P to the low P-plants. It is obvious that an adequate P nutrition is essential for the proper photosynthetic activity of plants.
Biological Nitrogen (N2) Fixation
Phosphorus has been found to be a key mineral nutrient responsible for an effective biological N2 fixation in leguminous plants. Under low P supply, nodulation and nodule functioning are impaired, and amount of N fixed is reduced.. Nodules represent a significant sink for P. It has been shown that P concentration of nodules of various legume plants is 3-fold higher compared to other parts of the plants (Schulze and Drevon, 2005, J. Exp. Bot. 56:1779–84; Qin et al., 2012, Plant Physiol. 159: 1634-1643; Lazai et al., 2017, Agron. J. 109:283–290). Qin et al (2012) showed that P deficiency significantly impairs nodulation in soybean plants and causes marked decreases nodule number and nodule size (Figure 4).When legume plants suffer from P deficiency, increasing amount of P is allocated in the nodules.
Figure 3: Changes in ATP formation and activities of ATP synthase enzyme in chloroplasts of barley plants grown under low and adequate P supply and also in P-deficient plants after re-supply of P (For the details see Carstensen et al.,2018, Plant Physiol 177:271–284)
There is often a close relationship between nodule formation and nodule P concentration. High dependency of N2 fixation to sufficient P nutrition is related to the fact that that N fixation process is a highly energy-demanding process and requires at least 16 moles ATP to reduce one mole N2. Hence, the activity of nitrogenase enzyme is also positively influenced by improving P nutritional status of plants. In whole nodules of soybean plants, the concentration of ATP and energy charge are significantly reduced under low P supply compared to the P sufficient conditions (Sa and Israel, 1991; Plant Physiol.97: 928-935). These findings highlight importance of P in optimal nodule performance and N fixation process.
Figure 4: Nodulation and nodule growth performance in soybean roots with low and adequate P application (Qin et al., 2012, Plant Physiol.. 159: 1634–1643)
Tillering, Leaf Expansion and Reproductive Growth
One of the main structural changes in response to low P availability in growth medium is the process of tiller development. Tillering and number of tillers are known to be major plant factors affecting yield capacity of cereals. Under low P supply, severe reduction or suppression of tillering is very common, depressing biomass and yield formation (Figure 5; Hammond and White, 2008, J Exp Bot 59: 93–109;). Similar to tillering, also leaf expansion is highly sensitive to P deficiency, and impairment in leaf expansion as a response to low P supply has been suggested to be the earliest change in P-deficient plants (Radin and Eidenbock, 1984, Plant Physiol 75: 372–377; Lynch et al., 1991; Crop Sci. 31: 380-387). As expected, a decrease in leaf area will diminish light interception and biomass production. Reduction in leaf expansion under low P supply has been ascribed to reduced transport of water from growth medium in the leaves and hence low turgor pressure needed for the expansion.
Figure 5: Wheat plants grown on a P-deficient soil with low, medium and adequate P fertilization (picture A. Yazici and I. Cakmak)
Phosphorus deficiency has also a clear negative impacts on reproductive growth of plants. Delay in reproductive development and retardation in ripening are common problems in plants under low P supply. However, according to Nord and Lynch (2008, Plant, Cell and Environ 31: 1432–1441), the well-known delay in flowering and maturity under P deficiency might be a useful delay for plants: it can allow plants to have longer time for the utilization and re-mobilization of P exiting in the vegetative tissues.
Phosphorus Deficiency Symptoms
Phosphorus deficiency symptoms commonly start on older leaves because of high phloem mobility of P within plants. Usually, visual P deficiency symptoms develop in leaves containing less than 0.2 percent P on a dry weight basis. Development of dark and bluish green colour on leaves is typical symptom of P deficiency in plants (Figure 6). When P deficiency is advanced, leaf chlorosis and leaf tip necrosis could be also visible. Under P deficient conditions, shoot growth is known to be more affected than the root growth, most probably, because P deficient plants allocate higher amounts of photoassimilates in the roots for better root formation and adaptation. This issue will be discussed in an another article.
Figure 6: Young maize plants grown in a medium with low and adequate P application (picture A. Yazici and I. Cakmak)
Today, most of agricultural soils have P deficiency problem limiting crop productivity, while in some regions P surpluses are common. Soil P deficiency problem is further aggravated through soil P depletion because of continuous cropping and soil erosion. Monitoring and measuring P nutritional status of plants by soil and plant tissue analysis is an important agronomic practice in reducing P deficiency-related impairments in plant growth. However, since soils tests are generally not useful, leaf tissue analysis results for P should be integrated with soil P tests. It is suggested that analysis of plants for the P status should be realized rather during early stage of growth. It is known that the level of P availability during the early stages of growth is highly critical and has a decisive effect on yield potential of crop plants (Grant et al., 2001, Can. J. Plant Sci. 81: 211–224).