Abstract
Background
Low phytoavailability of phosphorus (P) limits crop production worldwide. Increasing seed P content can improve plant establishment and increase yields. This is thought to be a consequence of faster initial root growth, which gives seedlings earlier access to growth-limiting resources, such as water and mineral elements. It can be calculated that seed P reserves can sustain maximal growth of cereal seedlings for several weeks after germination, until the plant has three or more leaves and an extensive root system.
Case study
In this issue of Plant and Soil, Muhammad Nadeem and colleagues report (1) that measurable P uptake by roots of maize seedlings begins about 5 d after germination, (2) that the commencement of root P uptake is coincident with the transition from carbon heterotrophy to carbon autotrophy, and (3) that neither the timing nor the rate of uptake of exogenous P by the developing root system is influenced by initial seed P content.
Hypothesis
Here it is hypothesised that the delay in P acquisition by roots of maize seedlings might be explained if the expression of genes encoding phosphate transporters is not upregulated either (1) because the plant has sufficient P for growth or (2) because a systemic signal from the shoot, which relies on photosynthesis or phloem development, is not produced, translocated or perceived.
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Phosphorus nutrition of annual crops
Annual crops exhibit a characteristic time course of P acquisition and internal P redistribution during their life cycle (Fig. 1; Hanway and Weber 1971; Hocking and Pate 1978; Hill 1980; Hocking and Steer 1983; Karlen et al. 1988; Feil et al. 1992; Hocking 1994; Manske et al. 2001; Masoni et al. 2007; Rose et al. 2007, 2008, 2010; Fageria et al. 2011). Seed P is the only P source available to sustain the initial growth of seedlings and, upon germination, seed P reserves are rapidly mobilized and translocated to emerging root and shoot tissues. This P source is subsequently supplemented by P uptake by the developing root system. Little is known about the physiological mechanisms controlling the transition between complete reliance on seed P reserves and the initiation of P acquisition by roots. Once seed P reserves are exhausted, plant growth must be supported by root P uptake alone, and the P concentrations in plant tissues are determined largely by the ability of the roots to acquire P from the soil and tissue growth rates (Lynch and Brown 2001; Manske et al. 2001; Aráujo and Teixeira 2003; Trehan and Sharma 2005; White et al. 2005; Parentoni and de Souza Júnior 2008; Hammond et al. 2009; Yaseen and Malhi 2009). If root P acquisition is insufficient to meet the P demand for new growth, characteristic biochemical, physiological and morphological responses occur both to improve the P economy of tissues and to increase P acquisition from the soil (Vance et al. 2003; Lynch 2007; White and Hammond 2008). Many of the responses of root tissues to P deficiency are co-ordinated by local and systemic signals involving gibberellins, auxin, cytokinins, ethylene and strigalactones, and the translocation of regulatory miRNAs and excess sucrose from the shoot to the root in the phloem (Hammond and White 2008, 2011; Vance 2010; Yang and Finnegan 2010; Chiou and Lin 2011; Lei et al. 2011). Increased sucrose supply to the root, in particular, is associated with the induction of greater P-uptake capacity in P deficient plants.
The P concentration in seeds of a mature plant varies with the phytoavailability of P in the soil and with environmental factors affecting plant growth and development. It also differs between plant species and between genotypes of the same plant species grown in the same environment (Schultz and French 1978). Chromosomal loci (QTL) affecting seed P concentration have been identified in several plant species including rice (Oryza sativa; Stangoulis et al. 2007; Garcia-Oliveira et al. 2009; Norton et al. 2010), common bean (Phaseolus vulgaris; Blair et al. 2009; Cichy et al. 2009a, b), Lotus japonicus (Klein and Grusak 2009), Arabidopsis thaliana (Bentsink et al. 2003; Waters and Grusak 2008), Brassica rapa (Zhao et al. 2007, 2008), and oilseed rape (Brassica napus; Ding et al. 2010). Between 30% and 90% of seed P occurs in the form of phytate (Table 1; Frossard et al. 2000; Reddy 2002; Raboy 2007, 2009). Phytate concentrations range from about 2 to 70 mg g−1 dry matter (DM) in seeds from various cereal and legume crops (Reddy 2002). Significant genetic variation in seed phytate concentration has been observed among commercial varieties of wheat, maize, barley, triticale, oats, rice, pearl millet and sorghum (White and Broadley 2009), and chromosomal loci (QTL) influencing seed phytate concentration have been identified in several plant species including rice (Stangoulis et al. 2007), common bean (Blair et al. 2009; Cichy et al. 2009ab), soybean (Walker et al. 2006; Maroof et al. 2009; Scaboo et al. 2009), Arabidopsis thaliana (Bentsink et al. 2003) and Brassica rapa (Zhao et al. 2007, 2008). Phytate typically accumulates in seeds as mixed salts of several cations, including K, Mg, Ca, Mn, Fe and Zn (Frossard et al. 2000; Reddy 2002; Raboy 2007, 2009; White and Broadley 2009). The activities of various phosphatases and phytases, already present in dry seeds, or synthesised de novo upon germination, effect phytate hydrolysis to provide the principal P source for developing seedlings (Dionisio et al. 2007, 2011).
Although the P contained in a seed contributes little to the final P content of the mature plant it produces, it contributes significantly to the P nutrition of a young seedling. Greater seed P reserves allow seedlings to establish faster and ultimately produce plants with higher yields (Bolland and Baker 1988; De Marco 1990; Zhang et al. 1990; Thompson et al. 1991; Thomson and Bolger 1993; Ros et al. 1997; Grant et al. 2001; Zhu and Smith 2001). Similarly, increasing seed P, for example by soaking in potassium phosphate solution, often, but not always, accelerates the growth of seedlings in P-deficient soils (Grant et al. 2001; Sekiya and Yano 2010). This is consistent with the beneficial effects of targeted early-season P-fertiliser applications, or the placement of P-fertilizers, on the establishment and yield of arable and horticultural crops (Grant et al. 2001; Burns et al. 2010). It is thought that a greater P supply from the seed promotes rapid root elongation, which gives seedlings earlier access to growth-limiting resources, such as water and mineral elements, thereby promoting resource acquisition and vigorous early growth (Grant et al. 2001).
The length of time that seed reserves can supply the P requirement of a seedling growing at its maximal rate in a particular environment can be calculated theoretically based on knowledge of the P content of the seed, the maximal growth rate, and the critical tissue P concentration required to sustain the maximal growth rate. Assuming a critical tissue P concentration of 2 mg P g−1 DM (White and Brown 2010), a small grain cereal, such as rye (Secale cereale), with a seed P content of 0.151 mg (Broadley et al. 2003; USDA-ARS 2011), a growth function of 1.4*e0.27t mg DM, where t is the number of days after germination, and a leaf appearance rate of 0.284 d−1 with an apparent start 1 d after germination at 20°C (White 1993), would have sufficient seed P reserves to support plant growth for 14.8 d, until after the appearance of the third leaf and the first tiller. The longest root might be about 30 cm long at this time (White 1993). For maize, seed P reserves would be sufficient to maintain maximal seedling growth for 17.5 d after germination assuming a similar tissue P requirement of 2 mg P g−1 DM, a seed P content of 0.952 mg (Nadeem et al. 2011b) and a growth function of 29*e0.16t mg DM at 28/25°C day/night (Pérez Leroux and Long 1994). This calculation can be compared with the observations of Nadeem et al. (2011a, b) that, when maize is grown at 25–28°C, (1) the average tissue P concentration has not fallen below 2 mg P g−1 DM even 4 weeks after germination, (2) seed P reserves alone can support maximal seedling growth in a medium lacking P for at least 4 weeks after germination, and (3) seed P is the only source of P for seedlings until about 1 week after germination when root P uptake begins to contribute. Similarly, Spinks and Barber (1948) observed no appreciable uptake of P by roots of wheat seedlings growing in unfertilised soil until they were at least 2 weeks old, and Schjørring and Jensén (1984) reported that seed P reserves could support maximal root growth of oilseed rape, barley and buckwheat (Fagopyrum esculentum) seedlings for at least 7 days at 20°C in a medium lacking P.
Relative contributions of seed P reserves and root P uptake to the P nutrition of seedlings
Two informative studies by Muhammad Nadeem and colleagues have been published recently in Plant and Soil (Nadeem et al. 2011a, b) quantifying the relative contributions of seed P reserves and root P uptake to the P requirements of young maize seedlings during establishment.
In the first of these papers, Nadeem et al. (2011a) observed that phytate, which contributed most of the seed P, was rapidly hydrolysed, but that hydrolyzed forms of P were temporarily stored in the seed before being translocated to the developing seedling (Nadeem et al. 2011a). This suggested to the authors that phytate hydrolysis did not limit P redistribution from seed to seedling (Nadeem et al. 2011a). They also observed that roots of seedlings growing at 25–28°C only began to take up significant amounts of P about 5 d after sowing, slightly earlier than the transition from carbon heterotrophy to carbon autotrophy, but seedlings continued to import seed P reserves for approximately 2 weeks until these were exhausted (Nadeem et al. 2011a, b). Thus, they concluded that seed P was the main P source during germination and initial seedling establishment.
In their second paper, Nadeem et al. (2011b) studied the influence of seed P content and exogenous P availability on the mobilisation of seed P reserves and induction of root P uptake by maize seedlings. They observed that the hydrolysis of phytate and the export of P from germinating seeds were both independent of exogenous P supply, but that the absolute rate of phytate hydrolysis was faster in seeds with greater phytate concentrations. They also observed that the amount of P contained in the seed did not influence the onset or rate of uptake of exogenous P by the developing root system. Phosphorus acquisition was determined solely by the P availability in the nutrient solution fed to the roots. They therefore concluded that the remobilization of seed P and the uptake of exogenous P by roots of maize seedlings were controlled independently.
It is often observed that phosphate uptake by roots is regulated systemically by plant P status (White 2012). It has been suggested that sucrose transported in the phloem from the shoot to the root acts as a systemic signal to regulate phosphate uptake by roots (Hammond and White 2008, 2011; Vance 2010; Lei et al. 2011). Thus, the expression of phosphate transporters increases (1) during the day, or under conditions of N or P deficiency, when more sucrose is translocated to the root, (2) when roots are supplied exogenous sucrose, and (3) in mutants overexpressing the SUC2 gene, which accumulate sucrose in their roots (Hammond and White 2008, 2011; Vance 2010; Lei et al. 2011). It is possible that roots of young seedlings do not take up phosphate either because the plant is P-replete or because there is no systemic sucrose signal. The theoretical calculations presented in the previous section, together with the empirical observations of Nadeem and colleagues, suggest that the P reserves of high-P maize seed (0.952 mg P seed−1) would be sufficient to maintain maximal growth of maize seedlings for 17.5 d, and that even the P reserves of low-P maize seed (0.506 mg P seed−1) would be sufficient to support maximal growth for 13.5 d at 25–28°C. However, it is also noteworthy that commencement of root P uptake was roughly coincident with the transition from carbon heterotrophy to carbon autotrophy (Nadeem et al. 2011a).
Classical studies indicated a basal temperature for leaf appearance in maize of 5–12°C (Duncan and Hesketh 1968; Tollenaar et al. 1979; Warrington and Kanemasu 1983) and a phyllochron of 22–66°C d (Tollenaar et al. 1979; Thiagarajah and Hunt 1982; Warrington and Kanemasu 1983). Assuming a basal temperature for leaf appearance of 10°C, a phyllochron of 60°C d, and an apparent start to leaf appearance after 2 d, the P reserves of high-P seed (0.952 mg P seed−1) and low-P seed (0.506 mg P seed−1) would suffice until the plant had 4.6 and 3.5 leaves, respectively (Fig. 2, line a). If the critical P concentration was greater than 2 mg P g−1 DM, then the leaf number at which the plant would begin to suffer from a lack of P (i.e. the critical phyllochron) would be reduced (Fig. 2, line b). For example, if the critical P concentration was 5 mg P g−1 DM, P reserves of 0.952 mg P seed-1 and 0.506 mg P seed−1 would suffice only until the plant had 2.9 and 1.7 leaves, respectively (Fig. 2, line b). If plant relative growth rate was lower, but the leaf production occurred at the same rate, seed P reserves would provide sufficient P for plant growth for a longer period (Fig. 2, line c). For example, if the critical P concentration was 2 mg P g−1 DM and the growth function was 29*e0.08t mg DM, the leaf number at which the plant would begin to suffer from a lack of P would be 9.9 and 7.5 in plants grown from seeds containing 0.952 mg P seed−1 and 0.506 mg P seed−1, respectively (Fig. 2, line c). This would equate to a plant of the same physiological age, but with smaller leaves and roots. Interestingly, P-replete seedlings of plant species from low P environments often have lower growth rates than those originating from high P environments (Bradshaw et al. 1960). Reducing seedling growth rates is, of course, not an agricultural solution for soils with low P availability, since it would result in reduced yields.
Contribution of seed reserves to the micronutrient nutrition of seedlings
In addition to supplying the seedling with P, seeds are a source of other essential elements required for plant growth, and the length of time that seed reserves can meet the requirements of a seedling growing at its maximal rate can be estimated (Table 2). It would appear that, with the exception of P, a wheat seedling, for example, growing at 20°C rapidly exhausts the supply of macronutrients in the seed. However, there are sufficient amounts of the micronutrients Fe, Zn, Mn, Cu, B, Ni and Mo in the seed to fulfil the requirements of the seedling for at least 2.5 phyllochrons after germination. This is a significant observation since it has been reported that increasing seed concentrations of micronutrient elements, such as Zn, Mn, Cu and Mo, often improves crop establishment and leads to increased yields on soils that have restricted phytoavailability of these elements (Brennan and Longnecker 2001; Brennan and Bolland 2007; Broadley et al. 2007; Malhi 2009). Greater seed reserves of micronutrients with low phytoavailabilty in the soil are likely to assist root system development, faster resource acquisition, and vigorous early growth.
Conclusions
It is evident from the foregoing discussion that seeds of crop plants generally contain sufficient P to support maximal growth of seedlings for several weeks after germination. This allows the development of an extensive root system, which must ultimately acquire the P required for continued plant growth. Greater seed P content enables seedlings to establish faster and, ultimately, to produce plants with higher yields. Significant P uptake by roots of several crop plants begins about a week after germination. The reason for this delay in P acquisition by roots is unknown. It might be attributed to limited access to phosphate in the rhizosphere or to a low abundance or activity of phosphate transporters in root epidermal cells. It is possible that the abundance of phosphate transporters in the root is developmentally regulated, or that the expression of genes encoding phosphate transporters is not upregulated in roots of young seedlings either (1) because the plant has sufficient P for growth or (2) because a systemic signal from the shoot, which relies on photosynthesis and phloem development, is not produced, translocated or perceived.
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Acknowledgements
We thank all participants at the international workshop on “Phosphorus: The Inside Story” held at the University of Western Australia in February 2011. Research by PJW is supported by the Rural and Environment Science and Analytical Services Division (RESAS) of the Scottish Government. We thank Dr Alison Bennett and Dr Paul Hallett for their comments on an original draft of the manuscript.
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White, P.J., Veneklaas, E.J. Nature and nurture: the importance of seed phosphorus content. Plant Soil 357, 1–8 (2012). https://doi.org/10.1007/s11104-012-1128-4
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DOI: https://doi.org/10.1007/s11104-012-1128-4